diff --git a/zebra-consensus/Cargo.toml b/zebra-consensus/Cargo.toml
index 86fabe3ce8a..2a60bddef0d 100644
--- a/zebra-consensus/Cargo.toml
+++ b/zebra-consensus/Cargo.toml
@@ -7,7 +7,10 @@ edition = "2021"
 
 [features]
 default = []
-getblocktemplate-rpcs = []
+getblocktemplate-rpcs = [
+     "zebra-state/getblocktemplate-rpcs", 
+     "zebra-chain/getblocktemplate-rpcs", 
+]
 proptest-impl = ["proptest", "proptest-derive", "zebra-chain/proptest-impl", "zebra-state/proptest-impl"]
 
 [dependencies]
diff --git a/zebra-consensus/src/block.rs b/zebra-consensus/src/block.rs
index a822323fe0d..231b4a94ba4 100644
--- a/zebra-consensus/src/block.rs
+++ b/zebra-consensus/src/block.rs
@@ -21,20 +21,17 @@ use thiserror::Error;
 use tower::{Service, ServiceExt};
 use tracing::Instrument;
 
-use zebra_chain::{
-    amount::Amount,
-    block::{self, Block},
-    parameters::Network,
-    transparent,
-    work::equihash,
-};
+use zebra_chain::{amount::Amount, block, parameters::Network, transparent, work::equihash};
 use zebra_state as zs;
 
 use crate::{error::*, transaction as tx, BoxError};
 
 pub mod check;
+pub mod request;
 pub mod subsidy;
 
+pub use request::Request;
+
 #[cfg(test)]
 mod tests;
 
@@ -74,6 +71,11 @@ pub enum VerifyBlockError {
     // TODO: make this into a concrete type, and add it to is_duplicate_request() (#2908)
     Commit(#[source] BoxError),
 
+    #[cfg(feature = "getblocktemplate-rpcs")]
+    #[error("unable to validate block proposal: failed semantic verification (proof of work is not checked for proposals)")]
+    // TODO: make this into a concrete type (see #5732)
+    ValidateProposal(#[source] BoxError),
+
     #[error("invalid transaction")]
     Transaction(#[from] TransactionError),
 }
@@ -115,7 +117,7 @@ where
     }
 }
 
-impl<S, V> Service<Arc<Block>> for BlockVerifier<S, V>
+impl<S, V> Service<Request> for BlockVerifier<S, V>
 where
     S: Service<zs::Request, Response = zs::Response, Error = BoxError> + Send + Clone + 'static,
     S::Future: Send + 'static,
@@ -134,11 +136,13 @@ where
         Poll::Ready(Ok(()))
     }
 
-    fn call(&mut self, block: Arc<Block>) -> Self::Future {
+    fn call(&mut self, request: Request) -> Self::Future {
         let mut state_service = self.state_service.clone();
         let mut transaction_verifier = self.transaction_verifier.clone();
         let network = self.network;
 
+        let block = request.block();
+
         // We don't include the block hash, because it's likely already in a parent span
         let span = tracing::debug_span!("block", height = ?block.coinbase_height());
 
@@ -172,10 +176,17 @@ where
                 Err(BlockError::MaxHeight(height, hash, block::Height::MAX))?;
             }
 
-            // Do the difficulty checks first, to raise the threshold for
-            // attacks that use any other fields.
-            check::difficulty_is_valid(&block.header, network, &height, &hash)?;
-            check::equihash_solution_is_valid(&block.header)?;
+            // > The block data MUST be validated and checked against the server's usual
+            // > acceptance rules (excluding the check for a valid proof-of-work).
+            // <https://en.bitcoin.it/wiki/BIP_0023#Block_Proposal>
+            if request.is_proposal() {
+                check::difficulty_threshold_is_valid(&block.header, network, &height, &hash)?;
+            } else {
+                // Do the difficulty checks first, to raise the threshold for
+                // attacks that use any other fields.
+                check::difficulty_is_valid(&block.header, network, &height, &hash)?;
+                check::equihash_solution_is_valid(&block.header)?;
+            }
 
             // Next, check the Merkle root validity, to ensure that
             // the header binds to the transactions in the blocks.
@@ -279,6 +290,23 @@ where
                 new_outputs,
                 transaction_hashes,
             };
+
+            // Return early for proposal requests when getblocktemplate-rpcs feature is enabled
+            #[cfg(feature = "getblocktemplate-rpcs")]
+            if request.is_proposal() {
+                return match state_service
+                    .ready()
+                    .await
+                    .map_err(VerifyBlockError::ValidateProposal)?
+                    .call(zs::Request::CheckBlockProposalValidity(prepared_block))
+                    .await
+                    .map_err(VerifyBlockError::ValidateProposal)?
+                {
+                    zs::Response::ValidBlockProposal => Ok(hash),
+                    _ => unreachable!("wrong response for CheckBlockProposalValidity"),
+                };
+            }
+
             match state_service
                 .ready()
                 .await
diff --git a/zebra-consensus/src/block/check.rs b/zebra-consensus/src/block/check.rs
index 094adf47b2c..ddd3dbefa63 100644
--- a/zebra-consensus/src/block/check.rs
+++ b/zebra-consensus/src/block/check.rs
@@ -58,24 +58,22 @@ pub fn coinbase_is_first(block: &Block) -> Result<Arc<transaction::Transaction>,
     Ok(first.clone())
 }
 
-/// Returns `Ok(())` if `hash` passes:
-///   - the target difficulty limit for `network` (PoWLimit), and
-///   - the difficulty filter,
-/// based on the fields in `header`.
+/// Returns `Ok(ExpandedDifficulty)` if the`difficulty_threshold` of `header` is at least as difficult as
+/// the target difficulty limit for `network` (PoWLimit)
 ///
-/// If the block is invalid, returns an error containing `height` and `hash`.
-pub fn difficulty_is_valid(
+/// If the header difficulty threshold is invalid, returns an error containing `height` and `hash`.
+pub fn difficulty_threshold_is_valid(
     header: &Header,
     network: Network,
     height: &Height,
     hash: &Hash,
-) -> Result<(), BlockError> {
+) -> Result<ExpandedDifficulty, BlockError> {
     let difficulty_threshold = header
         .difficulty_threshold
         .to_expanded()
         .ok_or(BlockError::InvalidDifficulty(*height, *hash))?;
 
-    // Note: the comparisons in this function are u256 integer comparisons, like
+    // Note: the comparison in this function is a u256 integer comparison, like
     // zcashd and bitcoin. Greater values represent *less* work.
 
     // The PowLimit check is part of `Threshold()` in the spec, but it doesn't
@@ -90,6 +88,26 @@ pub fn difficulty_is_valid(
         ))?;
     }
 
+    Ok(difficulty_threshold)
+}
+
+/// Returns `Ok(())` if `hash` passes:
+///   - the target difficulty limit for `network` (PoWLimit), and
+///   - the difficulty filter,
+/// based on the fields in `header`.
+///
+/// If the block is invalid, returns an error containing `height` and `hash`.
+pub fn difficulty_is_valid(
+    header: &Header,
+    network: Network,
+    height: &Height,
+    hash: &Hash,
+) -> Result<(), BlockError> {
+    let difficulty_threshold = difficulty_threshold_is_valid(header, network, height, hash)?;
+
+    // Note: the comparison in this function is a u256 integer comparison, like
+    // zcashd and bitcoin. Greater values represent *less* work.
+
     // # Consensus
     //
     // > The block MUST pass the difficulty filter.
diff --git a/zebra-consensus/src/block/request.rs b/zebra-consensus/src/block/request.rs
new file mode 100644
index 00000000000..9a0dbcc9cf9
--- /dev/null
+++ b/zebra-consensus/src/block/request.rs
@@ -0,0 +1,40 @@
+//! Block verifier request type.
+
+use std::sync::Arc;
+
+use zebra_chain::block::Block;
+
+#[derive(Debug, Clone, PartialEq, Eq)]
+/// A request to the chain or block verifier
+pub enum Request {
+    /// Performs semantic validation, then asks the state to perform contextual validation and commit the block
+    Commit(Arc<Block>),
+
+    #[cfg(feature = "getblocktemplate-rpcs")]
+    /// Performs semantic validation but skips checking proof of work,
+    /// then asks the state to perform contextual validation.
+    /// Does not commit the block to the state.
+    CheckProposal(Arc<Block>),
+}
+
+impl Request {
+    /// Returns inner block
+    pub fn block(&self) -> Arc<Block> {
+        Arc::clone(match self {
+            Request::Commit(block) => block,
+
+            #[cfg(feature = "getblocktemplate-rpcs")]
+            Request::CheckProposal(block) => block,
+        })
+    }
+
+    /// Returns `true` if the request is a proposal
+    pub fn is_proposal(&self) -> bool {
+        match self {
+            Request::Commit(_) => false,
+
+            #[cfg(feature = "getblocktemplate-rpcs")]
+            Request::CheckProposal(_) => true,
+        }
+    }
+}
diff --git a/zebra-consensus/src/block/tests.rs b/zebra-consensus/src/block/tests.rs
index 1901984541b..09512633b1c 100644
--- a/zebra-consensus/src/block/tests.rs
+++ b/zebra-consensus/src/block/tests.rs
@@ -28,19 +28,18 @@ use crate::{parameters::SLOW_START_SHIFT, transaction};
 
 use super::*;
 
-static VALID_BLOCK_TRANSCRIPT: Lazy<
-    Vec<(Arc<Block>, Result<block::Hash, ExpectedTranscriptError>)>,
-> = Lazy::new(|| {
-    let block: Arc<_> =
-        Block::zcash_deserialize(&zebra_test::vectors::BLOCK_MAINNET_GENESIS_BYTES[..])
-            .unwrap()
-            .into();
-    let hash = Ok(block.as_ref().into());
-    vec![(block, hash)]
-});
+static VALID_BLOCK_TRANSCRIPT: Lazy<Vec<(Request, Result<block::Hash, ExpectedTranscriptError>)>> =
+    Lazy::new(|| {
+        let block: Arc<_> =
+            Block::zcash_deserialize(&zebra_test::vectors::BLOCK_MAINNET_GENESIS_BYTES[..])
+                .unwrap()
+                .into();
+        let hash = Ok(block.as_ref().into());
+        vec![(Request::Commit(block), hash)]
+    });
 
 static INVALID_TIME_BLOCK_TRANSCRIPT: Lazy<
-    Vec<(Arc<Block>, Result<block::Hash, ExpectedTranscriptError>)>,
+    Vec<(Request, Result<block::Hash, ExpectedTranscriptError>)>,
 > = Lazy::new(|| {
     let mut block: Block =
         Block::zcash_deserialize(&zebra_test::vectors::BLOCK_MAINNET_GENESIS_BYTES[..]).unwrap();
@@ -55,11 +54,14 @@ static INVALID_TIME_BLOCK_TRANSCRIPT: Lazy<
         .unwrap();
     Arc::make_mut(&mut block.header).time = three_hours_in_the_future;
 
-    vec![(Arc::new(block), Err(ExpectedTranscriptError::Any))]
+    vec![(
+        Request::Commit(Arc::new(block)),
+        Err(ExpectedTranscriptError::Any),
+    )]
 });
 
 static INVALID_HEADER_SOLUTION_TRANSCRIPT: Lazy<
-    Vec<(Arc<Block>, Result<block::Hash, ExpectedTranscriptError>)>,
+    Vec<(Request, Result<block::Hash, ExpectedTranscriptError>)>,
 > = Lazy::new(|| {
     let mut block: Block =
         Block::zcash_deserialize(&zebra_test::vectors::BLOCK_MAINNET_GENESIS_BYTES[..]).unwrap();
@@ -67,11 +69,14 @@ static INVALID_HEADER_SOLUTION_TRANSCRIPT: Lazy<
     // Change nonce to something invalid
     Arc::make_mut(&mut block.header).nonce = [0; 32];
 
-    vec![(Arc::new(block), Err(ExpectedTranscriptError::Any))]
+    vec![(
+        Request::Commit(Arc::new(block)),
+        Err(ExpectedTranscriptError::Any),
+    )]
 });
 
 static INVALID_COINBASE_TRANSCRIPT: Lazy<
-    Vec<(Arc<Block>, Result<block::Hash, ExpectedTranscriptError>)>,
+    Vec<(Request, Result<block::Hash, ExpectedTranscriptError>)>,
 > = Lazy::new(|| {
     let header = block::Header::zcash_deserialize(&zebra_test::vectors::DUMMY_HEADER[..]).unwrap();
 
@@ -105,9 +110,18 @@ static INVALID_COINBASE_TRANSCRIPT: Lazy<
     assert_eq!(block3.transactions.len(), 2);
 
     vec![
-        (Arc::new(block1), Err(ExpectedTranscriptError::Any)),
-        (Arc::new(block2), Err(ExpectedTranscriptError::Any)),
-        (Arc::new(block3), Err(ExpectedTranscriptError::Any)),
+        (
+            Request::Commit(Arc::new(block1)),
+            Err(ExpectedTranscriptError::Any),
+        ),
+        (
+            Request::Commit(Arc::new(block2)),
+            Err(ExpectedTranscriptError::Any),
+        ),
+        (
+            Request::Commit(Arc::new(block3)),
+            Err(ExpectedTranscriptError::Any),
+        ),
     ]
 });
 
diff --git a/zebra-consensus/src/chain.rs b/zebra-consensus/src/chain.rs
index 59803180612..4f54f417768 100644
--- a/zebra-consensus/src/chain.rs
+++ b/zebra-consensus/src/chain.rs
@@ -15,7 +15,6 @@
 use std::{
     future::Future,
     pin::Pin,
-    sync::Arc,
     task::{Context, Poll},
 };
 
@@ -27,15 +26,14 @@ use tower::{buffer::Buffer, util::BoxService, Service, ServiceExt};
 use tracing::{instrument, Span};
 
 use zebra_chain::{
-    block::{self, Block, Height},
+    block::{self, Height},
     parameters::Network,
 };
 
 use zebra_state as zs;
 
 use crate::{
-    block::BlockVerifier,
-    block::VerifyBlockError,
+    block::{BlockVerifier, Request, VerifyBlockError},
     checkpoint::{CheckpointList, CheckpointVerifier, VerifyCheckpointError},
     error::TransactionError,
     transaction, BoxError, Config,
@@ -129,7 +127,7 @@ impl VerifyChainError {
     }
 }
 
-impl<S, V> Service<Arc<Block>> for ChainVerifier<S, V>
+impl<S, V> Service<Request> for ChainVerifier<S, V>
 where
     S: Service<zs::Request, Response = zs::Response, Error = BoxError> + Send + Clone + 'static,
     S::Future: Send + 'static,
@@ -167,14 +165,29 @@ where
         Poll::Ready(Ok(()))
     }
 
-    fn call(&mut self, block: Arc<Block>) -> Self::Future {
+    fn call(&mut self, request: Request) -> Self::Future {
+        let block = request.block();
+
         match block.coinbase_height() {
+            #[cfg(feature = "getblocktemplate-rpcs")]
+            // There's currently no known use case for block proposals below the checkpoint height,
+            // so it's okay to immediately return an error here.
+            Some(height) if height <= self.max_checkpoint_height && request.is_proposal() => {
+                async {
+                    // TODO: Add a `ValidateProposalError` enum with a `BelowCheckpoint` variant?
+                    Err(VerifyBlockError::ValidateProposal(
+                        "block proposals must be above checkpoint height".into(),
+                    ))?
+                }
+                .boxed()
+            }
+
             Some(height) if height <= self.max_checkpoint_height => {
                 self.checkpoint.call(block).map_err(Into::into).boxed()
             }
             // This also covers blocks with no height, which the block verifier
             // will reject immediately.
-            _ => self.block.call(block).map_err(Into::into).boxed(),
+            _ => self.block.call(request).map_err(Into::into).boxed(),
         }
     }
 }
@@ -219,7 +232,7 @@ pub async fn init<S>(
     mut state_service: S,
     debug_skip_parameter_preload: bool,
 ) -> (
-    Buffer<BoxService<Arc<Block>, block::Hash, VerifyChainError>, Arc<Block>>,
+    Buffer<BoxService<Request, block::Hash, VerifyChainError>, Request>,
     Buffer<
         BoxService<transaction::Request, transaction::Response, TransactionError>,
         transaction::Request,
diff --git a/zebra-consensus/src/chain/tests.rs b/zebra-consensus/src/chain/tests.rs
index 015e1d75f1a..308be754bdb 100644
--- a/zebra-consensus/src/chain/tests.rs
+++ b/zebra-consensus/src/chain/tests.rs
@@ -49,7 +49,7 @@ async fn verifiers_from_network(
     network: Network,
 ) -> (
     impl Service<
-            Arc<Block>,
+            Request,
             Response = block::Hash,
             Error = BoxError,
             Future = impl Future<Output = Result<block::Hash, BoxError>>,
@@ -77,7 +77,7 @@ async fn verifiers_from_network(
 }
 
 static BLOCK_VERIFY_TRANSCRIPT_GENESIS: Lazy<
-    Vec<(Arc<Block>, Result<block::Hash, ExpectedTranscriptError>)>,
+    Vec<(Request, Result<block::Hash, ExpectedTranscriptError>)>,
 > = Lazy::new(|| {
     let block: Arc<_> =
         Block::zcash_deserialize(&zebra_test::vectors::BLOCK_MAINNET_GENESIS_BYTES[..])
@@ -85,27 +85,29 @@ static BLOCK_VERIFY_TRANSCRIPT_GENESIS: Lazy<
             .into();
     let hash = Ok(block.hash());
 
-    vec![(block, hash)]
+    vec![(Request::Commit(block), hash)]
 });
 
 static BLOCK_VERIFY_TRANSCRIPT_GENESIS_FAIL: Lazy<
-    Vec<(Arc<Block>, Result<block::Hash, ExpectedTranscriptError>)>,
+    Vec<(Request, Result<block::Hash, ExpectedTranscriptError>)>,
 > = Lazy::new(|| {
     let block: Arc<_> =
         Block::zcash_deserialize(&zebra_test::vectors::BLOCK_MAINNET_GENESIS_BYTES[..])
             .unwrap()
             .into();
 
-    vec![(block, Err(ExpectedTranscriptError::Any))]
+    vec![(Request::Commit(block), Err(ExpectedTranscriptError::Any))]
 });
 
-static NO_COINBASE_TRANSCRIPT: Lazy<
-    Vec<(Arc<Block>, Result<block::Hash, ExpectedTranscriptError>)>,
-> = Lazy::new(|| {
-    let block = block_no_transactions();
+static NO_COINBASE_TRANSCRIPT: Lazy<Vec<(Request, Result<block::Hash, ExpectedTranscriptError>)>> =
+    Lazy::new(|| {
+        let block = block_no_transactions();
 
-    vec![(Arc::new(block), Err(ExpectedTranscriptError::Any))]
-});
+        vec![(
+            Request::Commit(Arc::new(block)),
+            Err(ExpectedTranscriptError::Any),
+        )]
+    });
 
 static NO_COINBASE_STATE_TRANSCRIPT: Lazy<
     Vec<(zs::Request, Result<zs::Response, ExpectedTranscriptError>)>,
diff --git a/zebra-consensus/src/lib.rs b/zebra-consensus/src/lib.rs
index 669e14dd83b..f07511d2a26 100644
--- a/zebra-consensus/src/lib.rs
+++ b/zebra-consensus/src/lib.rs
@@ -51,7 +51,7 @@ pub use block::{
         funding_streams::{funding_stream_address, funding_stream_values, new_coinbase_script},
         general::miner_subsidy,
     },
-    VerifyBlockError, MAX_BLOCK_SIGOPS,
+    Request, VerifyBlockError, MAX_BLOCK_SIGOPS,
 };
 pub use chain::VerifyChainError;
 pub use checkpoint::{
diff --git a/zebra-rpc/src/methods/get_block_template_rpcs.rs b/zebra-rpc/src/methods/get_block_template_rpcs.rs
index deac8245dff..10aeb96ffde 100644
--- a/zebra-rpc/src/methods/get_block_template_rpcs.rs
+++ b/zebra-rpc/src/methods/get_block_template_rpcs.rs
@@ -26,9 +26,8 @@ use crate::methods::{
             DEFAULT_SOLUTION_RATE_WINDOW_SIZE, GET_BLOCK_TEMPLATE_MEMPOOL_LONG_POLL_INTERVAL,
         },
         get_block_template::{
-            check_block_template_parameters, check_miner_address, check_synced_to_tip,
-            fetch_mempool_transactions, fetch_state_tip_and_local_time,
-            generate_coinbase_and_roots,
+            check_miner_address, check_synced_to_tip, fetch_mempool_transactions,
+            fetch_state_tip_and_local_time, generate_coinbase_and_roots, validate_block_proposal,
         },
         types::{
             get_block_template::GetBlockTemplate, get_mining_info, hex_data::HexData,
@@ -101,7 +100,7 @@ pub trait GetBlockTemplateRpc {
     fn get_block_template(
         &self,
         parameters: Option<get_block_template::JsonParameters>,
-    ) -> BoxFuture<Result<GetBlockTemplate>>;
+    ) -> BoxFuture<Result<get_block_template::Response>>;
 
     /// Submits block to the node to be validated and committed.
     /// Returns the [`submit_block::Response`] for the operation, as a JSON string.
@@ -165,7 +164,7 @@ where
         Response = zebra_state::ReadResponse,
         Error = zebra_state::BoxError,
     >,
-    ChainVerifier: Service<Arc<Block>, Response = block::Hash, Error = zebra_consensus::BoxError>
+    ChainVerifier: Service<zebra_consensus::Request, Response = block::Hash, Error = zebra_consensus::BoxError>
         + Clone
         + Send
         + Sync
@@ -217,7 +216,7 @@ where
         + Sync
         + 'static,
     Tip: ChainTip + Clone + Send + Sync + 'static,
-    ChainVerifier: Service<Arc<Block>, Response = block::Hash, Error = zebra_consensus::BoxError>
+    ChainVerifier: Service<zebra_consensus::Request, Response = block::Hash, Error = zebra_consensus::BoxError>
         + Clone
         + Send
         + Sync
@@ -265,12 +264,12 @@ where
         + 'static,
     <State as Service<zebra_state::ReadRequest>>::Future: Send,
     Tip: ChainTip + Clone + Send + Sync + 'static,
-    ChainVerifier: Service<Arc<Block>, Response = block::Hash, Error = zebra_consensus::BoxError>
+    ChainVerifier: Service<zebra_consensus::Request, Response = block::Hash, Error = zebra_consensus::BoxError>
         + Clone
         + Send
         + Sync
         + 'static,
-    <ChainVerifier as Service<Arc<Block>>>::Future: Send,
+    <ChainVerifier as Service<zebra_consensus::Request>>::Future: Send,
     SyncStatus: ChainSyncStatus + Clone + Send + Sync + 'static,
 {
     fn get_block_count(&self) -> Result<u32> {
@@ -312,11 +311,11 @@ where
         .boxed()
     }
 
-    // TODO: use HexData to handle block proposal data, and a generic error constructor (#5548)
+    // TODO: use a generic error constructor (#5548)
     fn get_block_template(
         &self,
         parameters: Option<get_block_template::JsonParameters>,
-    ) -> BoxFuture<Result<GetBlockTemplate>> {
+    ) -> BoxFuture<Result<get_block_template::Response>> {
         // Should we generate coinbase transactions that are exactly like zcashd's?
         //
         // This is useful for testing, but either way Zebra should obey the consensus rules.
@@ -332,21 +331,28 @@ where
         let sync_status = self.sync_status.clone();
         let state = self.state.clone();
 
+        if let Some(HexData(block_proposal_bytes)) = parameters
+            .as_ref()
+            .and_then(get_block_template::JsonParameters::block_proposal_data)
+        {
+            return validate_block_proposal(self.chain_verifier.clone(), block_proposal_bytes)
+                .boxed();
+        }
+
         // To implement long polling correctly, we split this RPC into multiple phases.
         async move {
+            get_block_template::check_parameters(&parameters)?;
+
+            let client_long_poll_id = parameters
+                .as_ref()
+                .and_then(|params| params.long_poll_id.clone());
+
             // - One-off checks
 
             // Check config and parameters.
             // These checks always have the same result during long polling.
             let miner_address = check_miner_address(miner_address)?;
 
-            let mut client_long_poll_id = None;
-            if let Some(parameters) = parameters {
-                check_block_template_parameters(&parameters)?;
-
-                client_long_poll_id = parameters.long_poll_id;
-            }
-
             // - Checks and fetches that can change during long polling
             //
             // Set up the loop.
@@ -506,7 +512,7 @@ where
                                     ?server_long_poll_id,
                                     ?client_long_poll_id,
                                     "returning from long poll due to a state error.\
-                                     Is Zebra shutting down?"
+                                    Is Zebra shutting down?"
                                 );
 
                                 return Err(Error {
@@ -582,7 +588,7 @@ where
                 COINBASE_LIKE_ZCASHD,
             );
 
-            Ok(response)
+            Ok(response.into())
         }
         .boxed()
     }
@@ -608,7 +614,7 @@ where
                     message: error.to_string(),
                     data: None,
                 })?
-                .call(Arc::new(block))
+                .call(zebra_consensus::Request::Commit(Arc::new(block)))
                 .await;
 
             let chain_error = match chain_verifier_response {
diff --git a/zebra-rpc/src/methods/get_block_template_rpcs/constants.rs b/zebra-rpc/src/methods/get_block_template_rpcs/constants.rs
index 1fcc28e5743..ed624e4dc83 100644
--- a/zebra-rpc/src/methods/get_block_template_rpcs/constants.rs
+++ b/zebra-rpc/src/methods/get_block_template_rpcs/constants.rs
@@ -18,6 +18,8 @@ pub const GET_BLOCK_TEMPLATE_MEMPOOL_LONG_POLL_INTERVAL: u64 = 5;
 pub const GET_BLOCK_TEMPLATE_NONCE_RANGE_FIELD: &str = "00000000ffffffff";
 
 /// A hardcoded list of fields that the miner can change from the block template.
+///
+/// <https://en.bitcoin.it/wiki/BIP_0023#Mutations>
 pub const GET_BLOCK_TEMPLATE_MUTABLE_FIELD: &[&str] = &[
     // Standard mutations, copied from zcashd
     "time",
@@ -26,8 +28,9 @@ pub const GET_BLOCK_TEMPLATE_MUTABLE_FIELD: &[&str] = &[
 ];
 
 /// A hardcoded list of Zebra's getblocktemplate RPC capabilities.
-/// Currently empty.
-pub const GET_BLOCK_TEMPLATE_CAPABILITIES_FIELD: &[&str] = &[];
+///
+/// <https://en.bitcoin.it/wiki/BIP_0023#Block_Proposal>
+pub const GET_BLOCK_TEMPLATE_CAPABILITIES_FIELD: &[&str] = &["proposal"];
 
 /// The max estimated distance to the chain tip for the getblocktemplate method.
 ///
@@ -35,6 +38,8 @@ pub const GET_BLOCK_TEMPLATE_CAPABILITIES_FIELD: &[&str] = &[];
 /// > A full validator MUST NOT accept blocks with nTime more than two hours in the future
 /// > according to its clock. This is not strictly a consensus rule because it is nondeterministic,
 /// > and clock time varies between nodes.
+/// >
+/// > <https://zips.z.cash/protocol/protocol.pdf#blockheader>
 pub const MAX_ESTIMATED_DISTANCE_TO_NETWORK_CHAIN_TIP: i32 = 100;
 
 /// The RPC error code used by `zcashd` for when it's still downloading initial blocks.
diff --git a/zebra-rpc/src/methods/get_block_template_rpcs/get_block_template.rs b/zebra-rpc/src/methods/get_block_template_rpcs/get_block_template.rs
index d2cfdb78549..7270e810f3c 100644
--- a/zebra-rpc/src/methods/get_block_template_rpcs/get_block_template.rs
+++ b/zebra-rpc/src/methods/get_block_template_rpcs/get_block_template.rs
@@ -8,12 +8,14 @@ use tower::{Service, ServiceExt};
 use zebra_chain::{
     amount::{self, Amount, NegativeOrZero, NonNegative},
     block::{
+        self,
         merkle::{self, AuthDataRoot},
         ChainHistoryBlockTxAuthCommitmentHash, Height,
     },
     chain_sync_status::ChainSyncStatus,
     chain_tip::ChainTip,
     parameters::Network,
+    serialization::ZcashDeserializeInto,
     transaction::{Transaction, UnminedTx, VerifiedUnminedTx},
     transparent,
 };
@@ -25,26 +27,57 @@ use zebra_state::GetBlockTemplateChainInfo;
 
 use crate::methods::get_block_template_rpcs::{
     constants::{MAX_ESTIMATED_DISTANCE_TO_NETWORK_CHAIN_TIP, NOT_SYNCED_ERROR_CODE},
-    types::{default_roots::DefaultRoots, get_block_template, transaction::TransactionTemplate},
+    types::{default_roots::DefaultRoots, transaction::TransactionTemplate},
 };
 
 pub use crate::methods::get_block_template_rpcs::types::get_block_template::*;
 
 // - Parameter checks
 
-/// Returns an error if the get block template RPC `parameters` are invalid.
-pub fn check_block_template_parameters(
-    parameters: &get_block_template::JsonParameters,
-) -> Result<()> {
-    if parameters.data.is_some() || parameters.mode == GetBlockTemplateRequestMode::Proposal {
-        return Err(Error {
+/// Checks that `data` is omitted in `Template` mode or provided in `Proposal` mode,
+///
+/// Returns an error if there's a mismatch between the mode and whether `data` is provided.
+pub fn check_parameters(parameters: &Option<JsonParameters>) -> Result<()> {
+    let Some(parameters) = parameters else {
+            return Ok(())
+        };
+
+    match parameters {
+        JsonParameters {
+            mode: GetBlockTemplateRequestMode::Template,
+            data: None,
+            ..
+        }
+        | JsonParameters {
+            mode: GetBlockTemplateRequestMode::Proposal,
+            data: Some(_),
+            ..
+        } => Ok(()),
+
+        JsonParameters {
+            mode: GetBlockTemplateRequestMode::Proposal,
+            data: None,
+            ..
+        } => Err(Error {
             code: ErrorCode::InvalidParams,
-            message: "\"proposal\" mode is currently unsupported by Zebra".to_string(),
+            message: "\"data\" parameter must be \
+                          provided in \"proposal\" mode"
+                .to_string(),
             data: None,
-        });
-    }
+        }),
 
-    Ok(())
+        JsonParameters {
+            mode: GetBlockTemplateRequestMode::Template,
+            data: Some(_),
+            ..
+        } => Err(Error {
+            code: ErrorCode::InvalidParams,
+            message: "\"data\" parameter must be \
+                          omitted in \"template\" mode"
+                .to_string(),
+            data: None,
+        }),
+    }
 }
 
 /// Returns the miner address, or an error if it is invalid.
@@ -60,6 +93,42 @@ pub fn check_miner_address(
     })
 }
 
+/// Attempts to validate block proposal against all of the server's
+/// usual acceptance rules (except proof-of-work).
+///
+/// Returns a `getblocktemplate` [`Response`].
+pub async fn validate_block_proposal<ChainVerifier>(
+    mut chain_verifier: ChainVerifier,
+    block_proposal_bytes: Vec<u8>,
+) -> Result<Response>
+where
+    ChainVerifier: Service<zebra_consensus::Request, Response = block::Hash, Error = zebra_consensus::BoxError>
+        + Clone
+        + Send
+        + Sync
+        + 'static,
+{
+    let Ok(block) = block_proposal_bytes.zcash_deserialize_into() else {
+         return Ok(ProposalRejectReason::Rejected.into())
+    };
+
+    let chain_verifier_response = chain_verifier
+        .ready()
+        .await
+        .map_err(|error| Error {
+            code: ErrorCode::ServerError(0),
+            message: error.to_string(),
+            data: None,
+        })?
+        .call(zebra_consensus::Request::CheckProposal(Arc::new(block)))
+        .await;
+
+    Ok(chain_verifier_response
+        .map(|_hash| ProposalResponse::Valid)
+        .unwrap_or_else(|_| ProposalRejectReason::Rejected.into())
+        .into())
+}
+
 // - State and syncer checks
 
 /// Returns an error if Zebra is not synced to the consensus chain tip.
diff --git a/zebra-rpc/src/methods/get_block_template_rpcs/types/get_block_template.rs b/zebra-rpc/src/methods/get_block_template_rpcs/types/get_block_template.rs
index 510871067d9..dcf62d32fa4 100644
--- a/zebra-rpc/src/methods/get_block_template_rpcs/types/get_block_template.rs
+++ b/zebra-rpc/src/methods/get_block_template_rpcs/types/get_block_template.rs
@@ -27,7 +27,7 @@ pub mod parameters;
 
 pub use parameters::*;
 
-/// A serialized `getblocktemplate` RPC response.
+/// A serialized `getblocktemplate` RPC response in template mode.
 #[derive(Clone, Debug, Eq, PartialEq, serde::Serialize, serde::Deserialize)]
 pub struct GetBlockTemplate {
     /// The getblocktemplate RPC capabilities supported by Zebra.
@@ -162,6 +162,14 @@ pub struct GetBlockTemplate {
 }
 
 impl GetBlockTemplate {
+    /// Returns a `Vec` of capabilities supported by the `getblocktemplate` RPC
+    pub fn capabilities() -> Vec<String> {
+        GET_BLOCK_TEMPLATE_CAPABILITIES_FIELD
+            .iter()
+            .map(ToString::to_string)
+            .collect()
+    }
+
     /// Returns a new [`GetBlockTemplate`] struct, based on the supplied arguments and defaults.
     ///
     /// The result of this method only depends on the supplied arguments and constants.
@@ -203,10 +211,7 @@ impl GetBlockTemplate {
             .expect("state always returns a valid difficulty value");
 
         // Convert default values
-        let capabilities: Vec<String> = GET_BLOCK_TEMPLATE_CAPABILITIES_FIELD
-            .iter()
-            .map(ToString::to_string)
-            .collect();
+        let capabilities: Vec<String> = Self::capabilities();
         let mutable: Vec<String> = GET_BLOCK_TEMPLATE_MUTABLE_FIELD
             .iter()
             .map(ToString::to_string)
@@ -253,3 +258,68 @@ impl GetBlockTemplate {
         }
     }
 }
+
+/// Error response to a `getblocktemplate` RPC request in proposal mode.
+#[derive(Debug, PartialEq, Eq, serde::Serialize, serde::Deserialize)]
+#[serde(rename_all = "kebab-case")]
+pub enum ProposalRejectReason {
+    /// Block proposal rejected as invalid.
+    Rejected,
+}
+
+/// Response to a `getblocktemplate` RPC request in proposal mode.
+///
+/// See <https://en.bitcoin.it/wiki/BIP_0023#Block_Proposal>
+#[derive(Debug, PartialEq, Eq, serde::Serialize, serde::Deserialize)]
+#[serde(untagged, rename_all = "kebab-case")]
+pub enum ProposalResponse {
+    /// Block proposal was rejected as invalid, returns `reject-reason` and server `capabilities`.
+    ErrorResponse {
+        /// Reason the proposal was invalid as-is.
+        reject_reason: ProposalRejectReason,
+
+        /// The getblocktemplate RPC capabilities supported by Zebra.
+        capabilities: Vec<String>,
+    },
+
+    /// Block proposal was successfully validated, returns null.
+    Valid,
+}
+
+#[derive(Debug, PartialEq, Eq, serde::Serialize, serde::Deserialize)]
+#[serde(untagged)]
+/// A `getblocktemplate` RPC response.
+pub enum Response {
+    /// `getblocktemplate` RPC request in template mode.
+    TemplateMode(Box<GetBlockTemplate>),
+
+    /// `getblocktemplate` RPC request in proposal mode.
+    ProposalMode(ProposalResponse),
+}
+
+impl From<ProposalRejectReason> for ProposalResponse {
+    fn from(reject_reason: ProposalRejectReason) -> Self {
+        Self::ErrorResponse {
+            reject_reason,
+            capabilities: GetBlockTemplate::capabilities(),
+        }
+    }
+}
+
+impl From<ProposalRejectReason> for Response {
+    fn from(error_response: ProposalRejectReason) -> Self {
+        Self::ProposalMode(ProposalResponse::from(error_response))
+    }
+}
+
+impl From<ProposalResponse> for Response {
+    fn from(proposal_response: ProposalResponse) -> Self {
+        Self::ProposalMode(proposal_response)
+    }
+}
+
+impl From<GetBlockTemplate> for Response {
+    fn from(template: GetBlockTemplate) -> Self {
+        Self::TemplateMode(Box::new(template))
+    }
+}
diff --git a/zebra-rpc/src/methods/get_block_template_rpcs/types/get_block_template/parameters.rs b/zebra-rpc/src/methods/get_block_template_rpcs/types/get_block_template/parameters.rs
index 01152891816..312ebf51f92 100644
--- a/zebra-rpc/src/methods/get_block_template_rpcs/types/get_block_template/parameters.rs
+++ b/zebra-rpc/src/methods/get_block_template_rpcs/types/get_block_template/parameters.rs
@@ -3,7 +3,6 @@
 use crate::methods::get_block_template_rpcs::types::{hex_data::HexData, long_poll::LongPollId};
 
 /// Defines whether the RPC method should generate a block template or attempt to validate a block proposal.
-/// `Proposal` mode is currently unsupported and will return an error.
 #[derive(Clone, Debug, serde::Deserialize, PartialEq, Eq)]
 #[serde(rename_all = "lowercase")]
 pub enum GetBlockTemplateRequestMode {
@@ -11,7 +10,6 @@ pub enum GetBlockTemplateRequestMode {
     Template,
 
     /// Indicates a request to validate block data.
-    /// Currently unsupported and will return an error.
     Proposal,
 }
 
@@ -63,19 +61,17 @@ pub enum GetBlockTemplateCapability {
 /// All other fields are optional.
 #[derive(Clone, Debug, PartialEq, Eq, serde::Deserialize, Default)]
 pub struct JsonParameters {
-    /// Must be set to "template" or omitted, as "proposal" mode is currently unsupported.
-    ///
     /// Defines whether the RPC method should generate a block template or attempt to
     /// validate block data, checking against all of the server's usual acceptance rules
     /// (excluding the check for a valid proof-of-work).
-    // TODO: Support `proposal` mode.
     #[serde(default)]
     pub mode: GetBlockTemplateRequestMode,
 
-    /// Must be omitted as "proposal" mode is currently unsupported.
+    /// Must be omitted when `getblocktemplate` RPC is called in "template" mode (or when `mode` is omitted).
+    /// Must be provided when `getblocktemplate` RPC is called in "proposal" mode.
     ///
     /// Hex-encoded block data to be validated and checked against the server's usual acceptance rules
-    /// (excluding the check for a valid proof-of-work) when `mode` is set to `proposal`.
+    /// (excluding the check for a valid proof-of-work).
     pub data: Option<HexData>,
 
     /// A list of client-side supported capability features
@@ -87,4 +83,29 @@ pub struct JsonParameters {
     /// In Zebra, the ID represents the chain tip, max time, and mempool contents.
     #[serde(rename = "longpollid")]
     pub long_poll_id: Option<LongPollId>,
+
+    /// The workid for the block template.
+    ///
+    /// currently unused.
+    #[serde(rename = "workid")]
+    pub _work_id: Option<String>,
+}
+
+impl JsonParameters {
+    /// Returns Some(data) with the block proposal hexdata if in `Proposal` mode and `data` is provided.
+    pub fn block_proposal_data(&self) -> Option<HexData> {
+        match self {
+            Self { data: None, .. }
+            | Self {
+                mode: GetBlockTemplateRequestMode::Template,
+                ..
+            } => None,
+
+            Self {
+                mode: GetBlockTemplateRequestMode::Proposal,
+                data,
+                ..
+            } => data.clone(),
+        }
+    }
 }
diff --git a/zebra-rpc/src/methods/tests/snapshot/get_block_template_rpcs.rs b/zebra-rpc/src/methods/tests/snapshot/get_block_template_rpcs.rs
index 2da8102dfb7..5a6108bac18 100644
--- a/zebra-rpc/src/methods/tests/snapshot/get_block_template_rpcs.rs
+++ b/zebra-rpc/src/methods/tests/snapshot/get_block_template_rpcs.rs
@@ -23,13 +23,16 @@ use zebra_node_services::mempool;
 
 use zebra_state::{GetBlockTemplateChainInfo, ReadRequest, ReadResponse};
 
-use zebra_test::mock_service::{MockService, PanicAssertion};
+use zebra_test::{
+    mock_service::{MockService, PanicAssertion},
+    vectors::BLOCK_MAINNET_1_BYTES,
+};
 
 use crate::methods::{
     get_block_template_rpcs::{
         self,
         types::{
-            get_block_template::{self, GetBlockTemplate},
+            get_block_template::{self, GetBlockTemplateRequestMode},
             get_mining_info,
             hex_data::HexData,
             long_poll::{LongPollId, LONG_POLL_ID_LENGTH},
@@ -159,12 +162,12 @@ pub async fn test_responses<State, ReadState>(
     // create a new rpc instance with new state and mock
     let get_block_template_rpc = GetBlockTemplateRpcImpl::new(
         network,
-        mining_config,
+        mining_config.clone(),
         Buffer::new(mempool.clone(), 1),
         new_read_state.clone(),
-        mock_chain_tip,
+        mock_chain_tip.clone(),
         chain_verifier,
-        mock_sync_status,
+        mock_sync_status.clone(),
     );
 
     // Basic variant (default mode and no extra features)
@@ -195,10 +198,12 @@ pub async fn test_responses<State, ReadState>(
         .await
         .respond(mempool::Response::FullTransactions(vec![]));
 
-    let get_block_template = get_block_template
+    let get_block_template::Response::TemplateMode(get_block_template) = get_block_template
         .await
         .expect("unexpected panic in getblocktemplate RPC task")
-        .expect("unexpected error in getblocktemplate RPC call");
+        .expect("unexpected error in getblocktemplate RPC call") else {
+            panic!("this getblocktemplate call without parameters should return the `TemplateMode` variant of the response")
+        };
 
     let coinbase_tx: Transaction = get_block_template
         .coinbase_txn
@@ -207,7 +212,12 @@ pub async fn test_responses<State, ReadState>(
         .zcash_deserialize_into()
         .expect("coinbase bytes are valid");
 
-    snapshot_rpc_getblocktemplate("basic", get_block_template, coinbase_tx, &settings);
+    snapshot_rpc_getblocktemplate(
+        "basic",
+        (*get_block_template).into(),
+        Some(coinbase_tx),
+        &settings,
+    );
 
     // long polling feature with submit old field
 
@@ -250,10 +260,12 @@ pub async fn test_responses<State, ReadState>(
         .await
         .respond(mempool::Response::FullTransactions(vec![]));
 
-    let get_block_template = get_block_template
+    let get_block_template::Response::TemplateMode(get_block_template) = get_block_template
         .await
         .expect("unexpected panic in getblocktemplate RPC task")
-        .expect("unexpected error in getblocktemplate RPC call");
+        .expect("unexpected error in getblocktemplate RPC call") else {
+            panic!("this getblocktemplate call without parameters should return the `TemplateMode` variant of the response")
+        };
 
     let coinbase_tx: Transaction = get_block_template
         .coinbase_txn
@@ -262,7 +274,62 @@ pub async fn test_responses<State, ReadState>(
         .zcash_deserialize_into()
         .expect("coinbase bytes are valid");
 
-    snapshot_rpc_getblocktemplate("long_poll", get_block_template, coinbase_tx, &settings);
+    snapshot_rpc_getblocktemplate(
+        "long_poll",
+        (*get_block_template).into(),
+        Some(coinbase_tx),
+        &settings,
+    );
+
+    // `getblocktemplate` proposal mode variant
+
+    let get_block_template = tokio::spawn(get_block_template_rpc.get_block_template(Some(
+        get_block_template::JsonParameters {
+            mode: GetBlockTemplateRequestMode::Proposal,
+            data: Some(HexData("".into())),
+            ..Default::default()
+        },
+    )));
+
+    let get_block_template = get_block_template
+        .await
+        .expect("unexpected panic in getblocktemplate RPC task")
+        .expect("unexpected error in getblocktemplate RPC call");
+
+    snapshot_rpc_getblocktemplate("invalid-proposal", get_block_template, None, &settings);
+
+    let mut mock_chain_verifier = MockService::build().for_unit_tests();
+    let get_block_template_rpc = GetBlockTemplateRpcImpl::new(
+        network,
+        mining_config,
+        Buffer::new(mempool.clone(), 1),
+        new_read_state.clone(),
+        mock_chain_tip,
+        mock_chain_verifier.clone(),
+        mock_sync_status,
+    );
+
+    let get_block_template = tokio::spawn(get_block_template_rpc.get_block_template(Some(
+        get_block_template::JsonParameters {
+            mode: GetBlockTemplateRequestMode::Proposal,
+            data: Some(HexData(BLOCK_MAINNET_1_BYTES.to_vec())),
+            ..Default::default()
+        },
+    )));
+
+    tokio::spawn(async move {
+        mock_chain_verifier
+            .expect_request_that(|req| matches!(req, zebra_consensus::Request::CheckProposal(_)))
+            .await
+            .respond(Hash::from([0; 32]));
+    });
+
+    let get_block_template = get_block_template
+        .await
+        .expect("unexpected panic in getblocktemplate RPC task")
+        .expect("unexpected error in getblocktemplate RPC call");
+
+    snapshot_rpc_getblocktemplate("proposal", get_block_template, None, &settings);
 
     // `submitblock`
 
@@ -287,19 +354,22 @@ fn snapshot_rpc_getblockhash(block_hash: GetBlockHash, settings: &insta::Setting
 /// Snapshot `getblocktemplate` response, using `cargo insta` and JSON serialization.
 fn snapshot_rpc_getblocktemplate(
     variant: &'static str,
-    block_template: GetBlockTemplate,
-    coinbase_tx: Transaction,
+    block_template: get_block_template::Response,
+    coinbase_tx: Option<Transaction>,
     settings: &insta::Settings,
 ) {
     settings.bind(|| {
         insta::assert_json_snapshot!(format!("get_block_template_{variant}"), block_template)
     });
-    settings.bind(|| {
-        insta::assert_ron_snapshot!(
-            format!("get_block_template_{variant}.coinbase_tx"),
-            coinbase_tx
-        )
-    });
+
+    if let Some(coinbase_tx) = coinbase_tx {
+        settings.bind(|| {
+            insta::assert_ron_snapshot!(
+                format!("get_block_template_{variant}.coinbase_tx"),
+                coinbase_tx
+            )
+        });
+    };
 }
 
 /// Snapshot `submitblock` response, using `cargo insta` and JSON serialization.
diff --git a/zebra-rpc/src/methods/tests/snapshot/snapshots/get_block_template_basic@mainnet_10.snap b/zebra-rpc/src/methods/tests/snapshot/snapshots/get_block_template_basic@mainnet_10.snap
index d0853e4a2ea..9506416935e 100644
--- a/zebra-rpc/src/methods/tests/snapshot/snapshots/get_block_template_basic@mainnet_10.snap
+++ b/zebra-rpc/src/methods/tests/snapshot/snapshots/get_block_template_basic@mainnet_10.snap
@@ -3,7 +3,9 @@ source: zebra-rpc/src/methods/tests/snapshot/get_block_template_rpcs.rs
 expression: block_template
 ---
 {
-  "capabilities": [],
+  "capabilities": [
+    "proposal"
+  ],
   "version": 4,
   "previousblockhash": "0000000000d723156d9b65ffcf4984da7a19675ed7e2f06d9e5d5188af087bf8",
   "blockcommitmentshash": "02990723c6b62a724651322d141b4a72a4ffd66518167d809badbd5117d5518a",
diff --git a/zebra-rpc/src/methods/tests/snapshot/snapshots/get_block_template_basic@testnet_10.snap b/zebra-rpc/src/methods/tests/snapshot/snapshots/get_block_template_basic@testnet_10.snap
index 0b6e9e0bd54..8a5dd4bc8f5 100644
--- a/zebra-rpc/src/methods/tests/snapshot/snapshots/get_block_template_basic@testnet_10.snap
+++ b/zebra-rpc/src/methods/tests/snapshot/snapshots/get_block_template_basic@testnet_10.snap
@@ -3,7 +3,9 @@ source: zebra-rpc/src/methods/tests/snapshot/get_block_template_rpcs.rs
 expression: block_template
 ---
 {
-  "capabilities": [],
+  "capabilities": [
+    "proposal"
+  ],
   "version": 4,
   "previousblockhash": "0000000000d723156d9b65ffcf4984da7a19675ed7e2f06d9e5d5188af087bf8",
   "blockcommitmentshash": "3b25791957f9383b6ce851d728a78309664d5d7a82ca87b6a9125a2f2c529792",
diff --git a/zebra-rpc/src/methods/tests/snapshot/snapshots/get_block_template_invalid-proposal@mainnet_10.snap b/zebra-rpc/src/methods/tests/snapshot/snapshots/get_block_template_invalid-proposal@mainnet_10.snap
new file mode 100644
index 00000000000..3a63ad3879a
--- /dev/null
+++ b/zebra-rpc/src/methods/tests/snapshot/snapshots/get_block_template_invalid-proposal@mainnet_10.snap
@@ -0,0 +1,10 @@
+---
+source: zebra-rpc/src/methods/tests/snapshot/get_block_template_rpcs.rs
+expression: block_template
+---
+{
+  "reject_reason": "rejected",
+  "capabilities": [
+    "proposal"
+  ]
+}
diff --git a/zebra-rpc/src/methods/tests/snapshot/snapshots/get_block_template_invalid-proposal@testnet_10.snap b/zebra-rpc/src/methods/tests/snapshot/snapshots/get_block_template_invalid-proposal@testnet_10.snap
new file mode 100644
index 00000000000..3a63ad3879a
--- /dev/null
+++ b/zebra-rpc/src/methods/tests/snapshot/snapshots/get_block_template_invalid-proposal@testnet_10.snap
@@ -0,0 +1,10 @@
+---
+source: zebra-rpc/src/methods/tests/snapshot/get_block_template_rpcs.rs
+expression: block_template
+---
+{
+  "reject_reason": "rejected",
+  "capabilities": [
+    "proposal"
+  ]
+}
diff --git a/zebra-rpc/src/methods/tests/snapshot/snapshots/get_block_template_long_poll@mainnet_10.snap b/zebra-rpc/src/methods/tests/snapshot/snapshots/get_block_template_long_poll@mainnet_10.snap
index 686028d69c8..043c937cd8b 100644
--- a/zebra-rpc/src/methods/tests/snapshot/snapshots/get_block_template_long_poll@mainnet_10.snap
+++ b/zebra-rpc/src/methods/tests/snapshot/snapshots/get_block_template_long_poll@mainnet_10.snap
@@ -3,7 +3,9 @@ source: zebra-rpc/src/methods/tests/snapshot/get_block_template_rpcs.rs
 expression: block_template
 ---
 {
-  "capabilities": [],
+  "capabilities": [
+    "proposal"
+  ],
   "version": 4,
   "previousblockhash": "0000000000d723156d9b65ffcf4984da7a19675ed7e2f06d9e5d5188af087bf8",
   "blockcommitmentshash": "02990723c6b62a724651322d141b4a72a4ffd66518167d809badbd5117d5518a",
diff --git a/zebra-rpc/src/methods/tests/snapshot/snapshots/get_block_template_long_poll@testnet_10.snap b/zebra-rpc/src/methods/tests/snapshot/snapshots/get_block_template_long_poll@testnet_10.snap
index ba44908e62e..e258d55e638 100644
--- a/zebra-rpc/src/methods/tests/snapshot/snapshots/get_block_template_long_poll@testnet_10.snap
+++ b/zebra-rpc/src/methods/tests/snapshot/snapshots/get_block_template_long_poll@testnet_10.snap
@@ -3,7 +3,9 @@ source: zebra-rpc/src/methods/tests/snapshot/get_block_template_rpcs.rs
 expression: block_template
 ---
 {
-  "capabilities": [],
+  "capabilities": [
+    "proposal"
+  ],
   "version": 4,
   "previousblockhash": "0000000000d723156d9b65ffcf4984da7a19675ed7e2f06d9e5d5188af087bf8",
   "blockcommitmentshash": "3b25791957f9383b6ce851d728a78309664d5d7a82ca87b6a9125a2f2c529792",
diff --git a/zebra-rpc/src/methods/tests/snapshot/snapshots/get_block_template_proposal@mainnet_10.snap b/zebra-rpc/src/methods/tests/snapshot/snapshots/get_block_template_proposal@mainnet_10.snap
new file mode 100644
index 00000000000..600686f4fe5
--- /dev/null
+++ b/zebra-rpc/src/methods/tests/snapshot/snapshots/get_block_template_proposal@mainnet_10.snap
@@ -0,0 +1,5 @@
+---
+source: zebra-rpc/src/methods/tests/snapshot/get_block_template_rpcs.rs
+expression: block_template
+---
+null
diff --git a/zebra-rpc/src/methods/tests/snapshot/snapshots/get_block_template_proposal@testnet_10.snap b/zebra-rpc/src/methods/tests/snapshot/snapshots/get_block_template_proposal@testnet_10.snap
new file mode 100644
index 00000000000..600686f4fe5
--- /dev/null
+++ b/zebra-rpc/src/methods/tests/snapshot/snapshots/get_block_template_proposal@testnet_10.snap
@@ -0,0 +1,5 @@
+---
+source: zebra-rpc/src/methods/tests/snapshot/get_block_template_rpcs.rs
+expression: block_template
+---
+null
diff --git a/zebra-rpc/src/methods/tests/vectors.rs b/zebra-rpc/src/methods/tests/vectors.rs
index dfadd172d15..a3615a7af6a 100644
--- a/zebra-rpc/src/methods/tests/vectors.rs
+++ b/zebra-rpc/src/methods/tests/vectors.rs
@@ -997,15 +997,16 @@ async fn rpc_getblocktemplate_mining_address(use_p2pkh: bool) {
     };
 
     let get_block_template_fut = get_block_template_rpc.get_block_template(None);
-
     let (get_block_template, ..) = tokio::join!(
         get_block_template_fut,
         mock_mempool_request_handler,
         mock_read_state_request_handler,
     );
 
-    let get_block_template =
-        get_block_template.expect("unexpected error in getblocktemplate RPC call");
+    let get_block_template::Response::TemplateMode(get_block_template) = get_block_template
+        .expect("unexpected error in getblocktemplate RPC call") else {
+            panic!("this getblocktemplate call without parameters should return the `TemplateMode` variant of the response")
+        };
 
     assert_eq!(
         get_block_template.capabilities,
@@ -1099,7 +1100,7 @@ async fn rpc_getblocktemplate_mining_address(use_p2pkh: bool) {
             ..Default::default()
         }))
         .await
-        .expect_err("needs an error when using unsupported mode");
+        .expect_err("needs an error when called in proposal mode without data");
 
     assert_eq!(get_block_template_sync_error.code, ErrorCode::InvalidParams);
 
@@ -1109,7 +1110,7 @@ async fn rpc_getblocktemplate_mining_address(use_p2pkh: bool) {
             ..Default::default()
         }))
         .await
-        .expect_err("needs an error when passing in block data");
+        .expect_err("needs an error when passing in block data in template mode");
 
     assert_eq!(get_block_template_sync_error.code, ErrorCode::InvalidParams);
 
diff --git a/zebra-rpc/src/server.rs b/zebra-rpc/src/server.rs
index bfa373e6cc0..d3548a0572e 100644
--- a/zebra-rpc/src/server.rs
+++ b/zebra-rpc/src/server.rs
@@ -7,7 +7,7 @@
 //! See the full list of
 //! [Differences between JSON-RPC 1.0 and 2.0.](https://www.simple-is-better.org/rpc/#differences-between-1-0-and-2-0)
 
-use std::{fmt, panic, sync::Arc};
+use std::{fmt, panic};
 
 use jsonrpc_core::{Compatibility, MetaIoHandler};
 use jsonrpc_http_server::{CloseHandle, ServerBuilder};
@@ -17,10 +17,7 @@ use tower::{buffer::Buffer, Service};
 use tracing::{Instrument, *};
 
 use zebra_chain::{
-    block::{self, Block},
-    chain_sync_status::ChainSyncStatus,
-    chain_tip::ChainTip,
-    parameters::Network,
+    block, chain_sync_status::ChainSyncStatus, chain_tip::ChainTip, parameters::Network,
 };
 use zebra_node_services::mempool;
 
@@ -107,12 +104,15 @@ impl RpcServer {
             + 'static,
         State::Future: Send,
         Tip: ChainTip + Clone + Send + Sync + 'static,
-        ChainVerifier: Service<Arc<Block>, Response = block::Hash, Error = zebra_consensus::BoxError>
-            + Clone
+        ChainVerifier: Service<
+                zebra_consensus::Request,
+                Response = block::Hash,
+                Error = zebra_consensus::BoxError,
+            > + Clone
             + Send
             + Sync
             + 'static,
-        <ChainVerifier as Service<Arc<Block>>>::Future: Send,
+        <ChainVerifier as Service<zebra_consensus::Request>>::Future: Send,
         SyncStatus: ChainSyncStatus + Clone + Send + Sync + 'static,
     {
         if let Some(listen_addr) = config.listen_addr {
diff --git a/zebra-state/src/request.rs b/zebra-state/src/request.rs
index c7f04eb79af..1ab59694f09 100644
--- a/zebra-state/src/request.rs
+++ b/zebra-state/src/request.rs
@@ -558,6 +558,13 @@ pub enum Request {
     ///
     /// Returns [`Response::ValidBestChainTipNullifiersAndAnchors`]
     CheckBestChainTipNullifiersAndAnchors(UnminedTx),
+
+    #[cfg(feature = "getblocktemplate-rpcs")]
+    /// Performs contextual validation of the given block, but does not commit it to the state.
+    ///
+    /// Returns [`Response::ValidBlockProposal`] when successful.
+    /// See `[ReadRequest::CheckBlockProposalValidity]` for details.
+    CheckBlockProposalValidity(PreparedBlock),
 }
 
 impl Request {
@@ -577,6 +584,8 @@ impl Request {
             Request::CheckBestChainTipNullifiersAndAnchors(_) => {
                 "best_chain_tip_nullifiers_anchors"
             }
+            #[cfg(feature = "getblocktemplate-rpcs")]
+            Request::CheckBlockProposalValidity(_) => "check_block_proposal_validity",
         }
     }
 
@@ -790,6 +799,16 @@ pub enum ReadRequest {
         /// Optionally estimate the network speed at the time when a certain block was found
         height: Option<block::Height>,
     },
+
+    #[cfg(feature = "getblocktemplate-rpcs")]
+    /// Performs contextual validation of the given block, but does not commit it to the state.
+    ///
+    /// It is the caller's responsibility to perform semantic validation.
+    /// (The caller does not need to check proof of work for block proposals.)
+    ///
+    /// Returns [`ReadResponse::ValidBlockProposal`] when successful, or an error if
+    /// the block fails contextual validation.
+    CheckBlockProposalValidity(PreparedBlock),
 }
 
 impl ReadRequest {
@@ -819,6 +838,8 @@ impl ReadRequest {
             ReadRequest::ChainInfo => "chain_info",
             #[cfg(feature = "getblocktemplate-rpcs")]
             ReadRequest::SolutionRate { .. } => "solution_rate",
+            #[cfg(feature = "getblocktemplate-rpcs")]
+            ReadRequest::CheckBlockProposalValidity(_) => "check_block_proposal_validity",
         }
     }
 
@@ -866,6 +887,11 @@ impl TryFrom<Request> for ReadRequest {
                 Err("ReadService does not write blocks")
             }
 
+            #[cfg(feature = "getblocktemplate-rpcs")]
+            Request::CheckBlockProposalValidity(prepared) => {
+                Ok(ReadRequest::CheckBlockProposalValidity(prepared))
+            }
+
             Request::AwaitUtxo(_) => Err("ReadService does not track pending UTXOs. \
                      Manually convert the request to ReadRequest::AnyChainUtxo, \
                      and handle pending UTXOs"),
diff --git a/zebra-state/src/response.rs b/zebra-state/src/response.rs
index 74386de9d90..1d529c2b991 100644
--- a/zebra-state/src/response.rs
+++ b/zebra-state/src/response.rs
@@ -59,6 +59,10 @@ pub enum Response {
     ///
     /// Does not check transparent UTXO inputs
     ValidBestChainTipNullifiersAndAnchors,
+
+    #[cfg(feature = "getblocktemplate-rpcs")]
+    /// Response to [`Request::CheckBlockProposalValidity`](crate::Request::CheckBlockProposalValidity)
+    ValidBlockProposal,
 }
 
 #[derive(Clone, Debug, PartialEq, Eq)]
@@ -137,6 +141,10 @@ pub enum ReadResponse {
     #[cfg(feature = "getblocktemplate-rpcs")]
     /// Response to [`ReadRequest::SolutionRate`](crate::ReadRequest::SolutionRate)
     SolutionRate(Option<u128>),
+
+    #[cfg(feature = "getblocktemplate-rpcs")]
+    /// Response to [`ReadRequest::CheckBlockProposalValidity`](crate::ReadRequest::CheckBlockProposalValidity)
+    ValidBlockProposal,
 }
 
 /// A structure with the information needed from the state to build a `getblocktemplate` RPC response.
@@ -215,6 +223,9 @@ impl TryFrom<ReadResponse> for Response {
                 Err("there is no corresponding Response for this ReadResponse")
             }
 
+            #[cfg(feature = "getblocktemplate-rpcs")]
+            ReadResponse::ValidBlockProposal => Ok(Response::ValidBlockProposal),
+
             #[cfg(feature = "getblocktemplate-rpcs")]
             ReadResponse::BlockHash(_) => {
                 Err("there is no corresponding Response for this ReadResponse")
diff --git a/zebra-state/src/service.rs b/zebra-state/src/service.rs
index b97f0652e5f..f155e0cb203 100644
--- a/zebra-state/src/service.rs
+++ b/zebra-state/src/service.rs
@@ -1047,6 +1047,24 @@ impl Service<Request> for StateService {
                 }
                 .boxed()
             }
+
+            #[cfg(feature = "getblocktemplate-rpcs")]
+            Request::CheckBlockProposalValidity(_) => {
+                // Redirect the request to the concurrent ReadStateService
+                let read_service = self.read_service.clone();
+
+                async move {
+                    let req = req
+                        .try_into()
+                        .expect("ReadRequest conversion should not fail");
+
+                    let rsp = read_service.oneshot(req).await?;
+                    let rsp = rsp.try_into().expect("Response conversion should not fail");
+
+                    Ok(rsp)
+                }
+                .boxed()
+            }
         }
     }
 }
@@ -1082,7 +1100,7 @@ impl Service<ReadRequest> for ReadStateService {
         Poll::Ready(Ok(()))
     }
 
-    #[instrument(name = "read_state", skip(self))]
+    #[instrument(name = "read_state", skip(self, req))]
     fn call(&mut self, req: ReadRequest) -> Self::Future {
         req.count_metric();
 
@@ -1688,6 +1706,58 @@ impl Service<ReadRequest> for ReadStateService {
                 .map(|join_result| join_result.expect("panic in ReadRequest::ChainInfo"))
                 .boxed()
             }
+
+            #[cfg(feature = "getblocktemplate-rpcs")]
+            ReadRequest::CheckBlockProposalValidity(prepared) => {
+                let timer = CodeTimer::start();
+
+                let state = self.clone();
+
+                // # Performance
+                //
+                // Allow other async tasks to make progress while concurrently reading blocks from disk.
+                let span = Span::current();
+                tokio::task::spawn_blocking(move || {
+                    span.in_scope(move || {
+                        tracing::info!("attempting to validate and commit block proposal onto a cloned non-finalized state");
+                        let mut latest_non_finalized_state = state.latest_non_finalized_state();
+
+                        // The previous block of a valid proposal must be on the best chain tip.
+                        let Some((_best_tip_height, best_tip_hash)) = read::best_tip(&latest_non_finalized_state, &state.db) else {
+                            return Err("state is empty: wait for Zebra to sync before submitting a proposal".into());
+                        };
+
+                        if prepared.block.header.previous_block_hash != best_tip_hash {
+                            return Err("proposal is not based on the current best chain tip: previous block hash must be the best chain tip".into());
+                        }
+
+                        // This clone of the non-finalized state is dropped when this closure returns.
+                        // The non-finalized state that's used in the rest of the state (including finalizing
+                        // blocks into the db) is not mutated here.
+                        //
+                        // TODO: Convert `CommitBlockError` to a new `ValidateProposalError`?
+                        latest_non_finalized_state.should_count_metrics = false;
+                        write::validate_and_commit_non_finalized(
+                            &state.db,
+                            &mut latest_non_finalized_state,
+                            prepared,
+                        )?;
+
+                        // The work is done in the future.
+                        timer.finish(
+                            module_path!(),
+                            line!(),
+                            "ReadRequest::CheckBlockProposalValidity",
+                        );
+
+                        Ok(ReadResponse::ValidBlockProposal)
+                    })
+                })
+                .map(|join_result| {
+                    join_result.expect("panic in ReadRequest::CheckBlockProposalValidity")
+                })
+                .boxed()
+            }
         }
     }
 }
diff --git a/zebra-state/src/service/check.rs b/zebra-state/src/service/check.rs
index 24db7846ead..d8e747964e4 100644
--- a/zebra-state/src/service/check.rs
+++ b/zebra-state/src/service/check.rs
@@ -14,7 +14,7 @@ use zebra_chain::{
 use crate::{
     service::{
         block_iter::any_ancestor_blocks, check::difficulty::POW_ADJUSTMENT_BLOCK_SPAN,
-        finalized_state::FinalizedState, non_finalized_state::NonFinalizedState,
+        finalized_state::ZebraDb, non_finalized_state::NonFinalizedState,
     },
     BoxError, PreparedBlock, ValidateContextError,
 };
@@ -365,25 +365,25 @@ where
 ///
 /// Additional contextual validity checks are performed by the non-finalized [`Chain`].
 pub(crate) fn initial_contextual_validity(
-    finalized_state: &FinalizedState,
+    finalized_state: &ZebraDb,
     non_finalized_state: &NonFinalizedState,
     prepared: &PreparedBlock,
 ) -> Result<(), ValidateContextError> {
     let relevant_chain = any_ancestor_blocks(
         non_finalized_state,
-        &finalized_state.db,
+        finalized_state,
         prepared.block.header.previous_block_hash,
     );
 
     // Security: check proof of work before any other checks
     check::block_is_valid_for_recent_chain(
         prepared,
-        finalized_state.network(),
-        finalized_state.db.finalized_tip_height(),
+        non_finalized_state.network,
+        finalized_state.finalized_tip_height(),
         relevant_chain,
     )?;
 
-    check::nullifier::no_duplicates_in_finalized_chain(prepared, &finalized_state.db)?;
+    check::nullifier::no_duplicates_in_finalized_chain(prepared, finalized_state)?;
 
     Ok(())
 }
diff --git a/zebra-state/src/service/check/tests/anchors.rs b/zebra-state/src/service/check/tests/anchors.rs
index f79c1ff896e..11564201e12 100644
--- a/zebra-state/src/service/check/tests/anchors.rs
+++ b/zebra-state/src/service/check/tests/anchors.rs
@@ -81,10 +81,12 @@ fn check_sprout_anchors() {
 
     // Validate and commit [`block_1`]. This will add an anchor referencing the
     // empty note commitment tree to the state.
-    assert!(
-        validate_and_commit_non_finalized(&finalized_state, &mut non_finalized_state, block_1)
-            .is_ok()
-    );
+    assert!(validate_and_commit_non_finalized(
+        &finalized_state.db,
+        &mut non_finalized_state,
+        block_1
+    )
+    .is_ok());
 
     let check_unmined_tx_anchors_result = unmined_txs.iter().try_for_each(|unmined_tx| {
         tx_anchors_refer_to_final_treestates(
@@ -98,7 +100,7 @@ fn check_sprout_anchors() {
 
     // Validate and commit [`block_2`]. This will also check the anchors.
     assert_eq!(
-        validate_and_commit_non_finalized(&finalized_state, &mut non_finalized_state, block_2),
+        validate_and_commit_non_finalized(&finalized_state.db, &mut non_finalized_state, block_2),
         Ok(())
     );
 }
@@ -288,10 +290,12 @@ fn check_sapling_anchors() {
         Err(ValidateContextError::UnknownSaplingAnchor { .. })
     ));
 
-    assert!(
-        validate_and_commit_non_finalized(&finalized_state, &mut non_finalized_state, block1)
-            .is_ok()
-    );
+    assert!(validate_and_commit_non_finalized(
+        &finalized_state.db,
+        &mut non_finalized_state,
+        block1
+    )
+    .is_ok());
 
     let check_unmined_tx_anchors_result = unmined_txs.iter().try_for_each(|unmined_tx| {
         tx_anchors_refer_to_final_treestates(
@@ -304,7 +308,7 @@ fn check_sapling_anchors() {
     assert!(check_unmined_tx_anchors_result.is_ok());
 
     assert_eq!(
-        validate_and_commit_non_finalized(&finalized_state, &mut non_finalized_state, block2),
+        validate_and_commit_non_finalized(&finalized_state.db, &mut non_finalized_state, block2),
         Ok(())
     );
 }
diff --git a/zebra-state/src/service/check/tests/nullifier.rs b/zebra-state/src/service/check/tests/nullifier.rs
index 3b1e43d343d..904426d4256 100644
--- a/zebra-state/src/service/check/tests/nullifier.rs
+++ b/zebra-state/src/service/check/tests/nullifier.rs
@@ -102,7 +102,7 @@ proptest! {
         } else {
             let block1 = Arc::new(block1).prepare();
             let commit_result = validate_and_commit_non_finalized(
-                &finalized_state,
+                &finalized_state.db,
                 &mut non_finalized_state,
                 block1.clone()
             );
@@ -156,7 +156,7 @@ proptest! {
 
         let block1 = Arc::new(block1).prepare();
         let commit_result = validate_and_commit_non_finalized(
-            &finalized_state,
+            &finalized_state.db,
             &mut non_finalized_state,
             block1
         );
@@ -217,7 +217,7 @@ proptest! {
 
         let block1 = Arc::new(block1).prepare();
         let commit_result = validate_and_commit_non_finalized(
-            &finalized_state,
+            &finalized_state.db,
             &mut non_finalized_state,
             block1
         );
@@ -278,8 +278,10 @@ proptest! {
 
         let block1 = Arc::new(block1).prepare();
         let commit_result = validate_and_commit_non_finalized(
-            &finalized_state,
-            &mut non_finalized_state,  block1);
+            &finalized_state.db,
+            &mut non_finalized_state,
+            block1
+        );
 
         prop_assert_eq!(
             commit_result,
@@ -364,7 +366,7 @@ proptest! {
         } else {
             let block1 = Arc::new(block1).prepare();
             let commit_result = validate_and_commit_non_finalized(
-                &finalized_state,
+                &finalized_state.db,
                 &mut non_finalized_state,
                 block1.clone()
             );
@@ -383,7 +385,7 @@ proptest! {
 
         let block2 = Arc::new(block2).prepare();
         let commit_result = validate_and_commit_non_finalized(
-            &finalized_state,
+            &finalized_state.db,
             &mut non_finalized_state,
             block2
         );
@@ -459,8 +461,10 @@ proptest! {
         } else {
             let block1 = Arc::new(block1).prepare();
             let commit_result = validate_and_commit_non_finalized(
-            &finalized_state,
-            &mut non_finalized_state,  block1.clone());
+                &finalized_state.db,
+                &mut non_finalized_state,
+                block1.clone()
+            );
 
             prop_assert_eq!(commit_result, Ok(()));
             prop_assert_eq!(Some((Height(1), block1.hash)), read::best_tip(&non_finalized_state, &finalized_state.db));
@@ -506,8 +510,10 @@ proptest! {
 
         let block1 = Arc::new(block1).prepare();
         let commit_result = validate_and_commit_non_finalized(
-            &finalized_state,
-            &mut non_finalized_state,  block1);
+            &finalized_state.db,
+            &mut non_finalized_state,
+            block1
+        );
 
         prop_assert_eq!(
             commit_result,
@@ -560,7 +566,7 @@ proptest! {
 
         let block1 = Arc::new(block1).prepare();
         let commit_result = validate_and_commit_non_finalized(
-            &finalized_state,
+            &finalized_state.db,
             &mut non_finalized_state,
             block1
         );
@@ -639,8 +645,10 @@ proptest! {
         } else {
             let block1 = Arc::new(block1).prepare();
             let commit_result = validate_and_commit_non_finalized(
-            &finalized_state,
-            &mut non_finalized_state,  block1.clone());
+                &finalized_state.db,
+                &mut non_finalized_state,
+                block1.clone()
+            );
 
             prop_assert_eq!(commit_result, Ok(()));
             prop_assert_eq!(Some((Height(1), block1.hash)), read::best_tip(&non_finalized_state, &finalized_state.db));
@@ -655,8 +663,10 @@ proptest! {
 
         let block2 = Arc::new(block2).prepare();
         let commit_result = validate_and_commit_non_finalized(
-            &finalized_state,
-            &mut non_finalized_state,  block2);
+            &finalized_state.db,
+            &mut non_finalized_state,
+            block2
+        );
 
         prop_assert_eq!(
             commit_result,
@@ -731,8 +741,10 @@ proptest! {
         } else {
             let block1 = Arc::new(block1).prepare();
             let commit_result = validate_and_commit_non_finalized(
-            &finalized_state,
-            &mut non_finalized_state,  block1.clone());
+                &finalized_state.db,
+                &mut non_finalized_state,
+                block1.clone()
+            );
 
             prop_assert_eq!(commit_result, Ok(()));
             prop_assert_eq!(Some((Height(1), block1.hash)), read::best_tip(&non_finalized_state, &finalized_state.db));
@@ -779,8 +791,10 @@ proptest! {
 
         let block1 = Arc::new(block1).prepare();
         let commit_result = validate_and_commit_non_finalized(
-            &finalized_state,
-            &mut non_finalized_state,  block1);
+            &finalized_state.db,
+            &mut non_finalized_state,
+            block1
+        );
 
         prop_assert_eq!(
             commit_result,
@@ -837,8 +851,10 @@ proptest! {
 
         let block1 = Arc::new(block1).prepare();
         let commit_result = validate_and_commit_non_finalized(
-            &finalized_state,
-            &mut non_finalized_state,  block1);
+            &finalized_state.db,
+            &mut non_finalized_state,
+            block1
+        );
 
         prop_assert_eq!(
             commit_result,
@@ -918,8 +934,10 @@ proptest! {
         } else {
             let block1 = Arc::new(block1).prepare();
             let commit_result = validate_and_commit_non_finalized(
-            &finalized_state,
-            &mut non_finalized_state,  block1.clone());
+                &finalized_state.db,
+                &mut non_finalized_state,
+                block1.clone()
+            );
 
             prop_assert_eq!(commit_result, Ok(()));
             prop_assert_eq!(Some((Height(1), block1.hash)), read::best_tip(&non_finalized_state, &finalized_state.db));
@@ -933,8 +951,10 @@ proptest! {
 
         let block2 = Arc::new(block2).prepare();
         let commit_result = validate_and_commit_non_finalized(
-            &finalized_state,
-            &mut non_finalized_state,  block2);
+            &finalized_state.db,
+            &mut non_finalized_state,
+            block2
+        );
 
         prop_assert_eq!(
             commit_result,
diff --git a/zebra-state/src/service/check/tests/utxo.rs b/zebra-state/src/service/check/tests/utxo.rs
index efb70c66504..6d14b8a13dd 100644
--- a/zebra-state/src/service/check/tests/utxo.rs
+++ b/zebra-state/src/service/check/tests/utxo.rs
@@ -194,8 +194,10 @@ proptest! {
         } else {
             let block1 = Arc::new(block1).prepare();
             let commit_result = validate_and_commit_non_finalized(
-            &finalized_state,
-            &mut non_finalized_state,  block1.clone());
+                &finalized_state.db,
+                &mut non_finalized_state,
+                block1.clone()
+            );
 
             // the block was committed
             prop_assert_eq!(commit_result, Ok(()));
@@ -279,8 +281,10 @@ proptest! {
         } else {
             let block2 = Arc::new(block2).prepare();
             let commit_result = validate_and_commit_non_finalized(
-            &finalized_state,
-            &mut non_finalized_state,  block2.clone());
+                &finalized_state.db,
+                &mut non_finalized_state,
+                block2.clone()
+            );
 
             // the block was committed
             prop_assert_eq!(commit_result, Ok(()));
@@ -357,8 +361,10 @@ proptest! {
 
         let block1 = Arc::new(block1).prepare();
         let commit_result = validate_and_commit_non_finalized(
-            &finalized_state,
-            &mut non_finalized_state,  block1);
+            &finalized_state.db,
+            &mut non_finalized_state,
+            block1
+        );
 
         // the block was rejected
         prop_assert_eq!(
@@ -419,8 +425,10 @@ proptest! {
 
         let block2 = Arc::new(block2).prepare();
         let commit_result = validate_and_commit_non_finalized(
-            &finalized_state,
-            &mut non_finalized_state,  block2);
+            &finalized_state.db,
+            &mut non_finalized_state,
+            block2
+        );
 
         // the block was rejected
         prop_assert_eq!(
@@ -503,8 +511,10 @@ proptest! {
 
         let block2 = Arc::new(block2).prepare();
         let commit_result = validate_and_commit_non_finalized(
-            &finalized_state,
-            &mut non_finalized_state,  block2);
+            &finalized_state.db,
+            &mut non_finalized_state,
+            block2
+        );
 
         // the block was rejected
         prop_assert_eq!(
@@ -615,8 +625,10 @@ proptest! {
         } else {
             let block2 = block2.clone().prepare();
             let commit_result = validate_and_commit_non_finalized(
-            &finalized_state,
-            &mut non_finalized_state,  block2.clone());
+                &finalized_state.db,
+                &mut non_finalized_state,
+                block2.clone()
+            );
 
             // the block was committed
             prop_assert_eq!(commit_result, Ok(()));
@@ -651,8 +663,10 @@ proptest! {
 
         let block3 = Arc::new(block3).prepare();
         let commit_result = validate_and_commit_non_finalized(
-            &finalized_state,
-            &mut non_finalized_state,  block3);
+            &finalized_state.db,
+            &mut non_finalized_state,
+            block3
+        );
 
         // the block was rejected
         if use_finalized_state_spend {
@@ -725,8 +739,10 @@ proptest! {
 
         let block1 = Arc::new(block1).prepare();
         let commit_result = validate_and_commit_non_finalized(
-            &finalized_state,
-            &mut non_finalized_state,  block1);
+            &finalized_state.db,
+            &mut non_finalized_state,
+            block1
+        );
 
         // the block was rejected
         prop_assert_eq!(
@@ -790,8 +806,10 @@ proptest! {
 
         let block1 = Arc::new(block1).prepare();
         let commit_result = validate_and_commit_non_finalized(
-            &finalized_state,
-            &mut non_finalized_state,  block1);
+            &finalized_state.db,
+            &mut non_finalized_state,
+            block1
+        );
 
         // the block was rejected
         prop_assert_eq!(
@@ -885,7 +903,7 @@ fn new_state_with_mainnet_transparent_data(
     } else {
         let block1 = block1.clone().prepare();
         let commit_result = validate_and_commit_non_finalized(
-            &finalized_state,
+            &finalized_state.db,
             &mut non_finalized_state,
             block1.clone(),
         );
diff --git a/zebra-state/src/service/non_finalized_state.rs b/zebra-state/src/service/non_finalized_state.rs
index 74fb3d7ff25..3e343da7405 100644
--- a/zebra-state/src/service/non_finalized_state.rs
+++ b/zebra-state/src/service/non_finalized_state.rs
@@ -44,9 +44,14 @@ pub struct NonFinalizedState {
     pub chain_set: BTreeSet<Arc<Chain>>,
 
     /// The configured Zcash network.
-    //
-    // Note: this field is currently unused, but it's useful for debugging.
     pub network: Network,
+
+    #[cfg(feature = "getblocktemplate-rpcs")]
+    /// Configures the non-finalized state to count metrics.
+    ///
+    /// Used for skipping metrics counting when testing block proposals
+    /// with a commit to a cloned non-finalized state.
+    pub should_count_metrics: bool,
 }
 
 impl NonFinalizedState {
@@ -55,6 +60,8 @@ impl NonFinalizedState {
         NonFinalizedState {
             chain_set: Default::default(),
             network,
+            #[cfg(feature = "getblocktemplate-rpcs")]
+            should_count_metrics: true,
         }
     }
 
@@ -494,6 +501,11 @@ impl NonFinalizedState {
 
     /// Update the metrics after `block` is committed
     fn update_metrics_for_committed_block(&self, height: block::Height, hash: block::Hash) {
+        #[cfg(feature = "getblocktemplate-rpcs")]
+        if !self.should_count_metrics {
+            return;
+        }
+
         metrics::counter!("state.memory.committed.block.count", 1);
         metrics::gauge!("state.memory.committed.block.height", height.0 as f64);
 
@@ -517,6 +529,11 @@ impl NonFinalizedState {
 
     /// Update the metrics after `self.chain_set` is modified
     fn update_metrics_for_chains(&self) {
+        #[cfg(feature = "getblocktemplate-rpcs")]
+        if !self.should_count_metrics {
+            return;
+        }
+
         metrics::gauge!("state.memory.chain.count", self.chain_set.len() as f64);
         metrics::gauge!(
             "state.memory.best.chain.length",
diff --git a/zebra-state/src/service/write.rs b/zebra-state/src/service/write.rs
index 5ba92218431..8f33af7b6d1 100644
--- a/zebra-state/src/service/write.rs
+++ b/zebra-state/src/service/write.rs
@@ -12,7 +12,7 @@ use crate::{
     constants::MAX_BLOCK_REORG_HEIGHT,
     service::{
         check,
-        finalized_state::FinalizedState,
+        finalized_state::{FinalizedState, ZebraDb},
         non_finalized_state::NonFinalizedState,
         queued_blocks::{QueuedFinalized, QueuedNonFinalized},
         BoxError, ChainTipBlock, ChainTipSender, CloneError,
@@ -36,17 +36,17 @@ const PARENT_ERROR_MAP_LIMIT: usize = MAX_BLOCK_REORG_HEIGHT as usize * 2;
 /// non-finalized state if it is contextually valid.
 #[tracing::instrument(level = "debug", skip(prepared), fields(height = ?prepared.height, hash = %prepared.hash))]
 pub(crate) fn validate_and_commit_non_finalized(
-    finalized_state: &FinalizedState,
+    finalized_state: &ZebraDb,
     non_finalized_state: &mut NonFinalizedState,
     prepared: PreparedBlock,
 ) -> Result<(), CommitBlockError> {
     check::initial_contextual_validity(finalized_state, non_finalized_state, &prepared)?;
     let parent_hash = prepared.block.header.previous_block_hash;
 
-    if finalized_state.db.finalized_tip_hash() == parent_hash {
-        non_finalized_state.commit_new_chain(prepared, &finalized_state.db)?;
+    if finalized_state.finalized_tip_hash() == parent_hash {
+        non_finalized_state.commit_new_chain(prepared, finalized_state)?;
     } else {
-        non_finalized_state.commit_block(prepared, &finalized_state.db)?;
+        non_finalized_state.commit_block(prepared, finalized_state)?;
     }
 
     Ok(())
@@ -205,7 +205,7 @@ pub fn write_blocks_from_channels(
         } else {
             tracing::trace!(?child_hash, "validating queued child");
             result = validate_and_commit_non_finalized(
-                &finalized_state,
+                &finalized_state.db,
                 &mut non_finalized_state,
                 queued_child,
             )
diff --git a/zebrad/src/components/inbound.rs b/zebrad/src/components/inbound.rs
index 36a121e6dd1..57a7b4f3b1d 100644
--- a/zebrad/src/components/inbound.rs
+++ b/zebrad/src/components/inbound.rs
@@ -24,10 +24,7 @@ use tower::{buffer::Buffer, timeout::Timeout, util::BoxService, Service, Service
 use zebra_network as zn;
 use zebra_state as zs;
 
-use zebra_chain::{
-    block::{self, Block},
-    transaction::UnminedTxId,
-};
+use zebra_chain::{block, transaction::UnminedTxId};
 use zebra_consensus::chain::VerifyChainError;
 use zebra_network::{
     constants::{ADDR_RESPONSE_LIMIT_DENOMINATOR, MAX_ADDRS_IN_MESSAGE},
@@ -53,7 +50,10 @@ type BlockDownloadPeerSet =
     Buffer<BoxService<zn::Request, zn::Response, zn::BoxError>, zn::Request>;
 type State = Buffer<BoxService<zs::Request, zs::Response, zs::BoxError>, zs::Request>;
 type Mempool = Buffer<BoxService<mempool::Request, mempool::Response, BoxError>, mempool::Request>;
-type BlockVerifier = Buffer<BoxService<Arc<Block>, block::Hash, VerifyChainError>, Arc<Block>>;
+type BlockVerifier = Buffer<
+    BoxService<zebra_consensus::Request, block::Hash, VerifyChainError>,
+    zebra_consensus::Request,
+>;
 type GossipedBlockDownloads =
     BlockDownloads<Timeout<BlockDownloadPeerSet>, Timeout<BlockVerifier>, State>;
 
diff --git a/zebrad/src/components/inbound/downloads.rs b/zebrad/src/components/inbound/downloads.rs
index 250b904831f..130d324ba45 100644
--- a/zebrad/src/components/inbound/downloads.rs
+++ b/zebrad/src/components/inbound/downloads.rs
@@ -4,7 +4,6 @@ use std::{
     collections::HashMap,
     convert::TryFrom,
     pin::Pin,
-    sync::Arc,
     task::{Context, Poll},
 };
 
@@ -18,10 +17,7 @@ use tokio::{sync::oneshot, task::JoinHandle};
 use tower::{Service, ServiceExt};
 use tracing_futures::Instrument;
 
-use zebra_chain::{
-    block::{self, Block},
-    chain_tip::ChainTip,
-};
+use zebra_chain::{block, chain_tip::ChainTip};
 use zebra_network as zn;
 use zebra_state as zs;
 
@@ -77,7 +73,10 @@ pub struct Downloads<ZN, ZV, ZS>
 where
     ZN: Service<zn::Request, Response = zn::Response, Error = BoxError> + Send + Clone + 'static,
     ZN::Future: Send,
-    ZV: Service<Arc<Block>, Response = block::Hash, Error = BoxError> + Send + Clone + 'static,
+    ZV: Service<zebra_consensus::Request, Response = block::Hash, Error = BoxError>
+        + Send
+        + Clone
+        + 'static,
     ZV::Future: Send,
     ZS: Service<zs::Request, Response = zs::Response, Error = BoxError> + Send + Clone + 'static,
     ZS::Future: Send,
@@ -117,7 +116,10 @@ impl<ZN, ZV, ZS> Stream for Downloads<ZN, ZV, ZS>
 where
     ZN: Service<zn::Request, Response = zn::Response, Error = BoxError> + Send + Clone + 'static,
     ZN::Future: Send,
-    ZV: Service<Arc<Block>, Response = block::Hash, Error = BoxError> + Send + Clone + 'static,
+    ZV: Service<zebra_consensus::Request, Response = block::Hash, Error = BoxError>
+        + Send
+        + Clone
+        + 'static,
     ZV::Future: Send,
     ZS: Service<zs::Request, Response = zs::Response, Error = BoxError> + Send + Clone + 'static,
     ZS::Future: Send,
@@ -160,7 +162,10 @@ impl<ZN, ZV, ZS> Downloads<ZN, ZV, ZS>
 where
     ZN: Service<zn::Request, Response = zn::Response, Error = BoxError> + Send + Clone + 'static,
     ZN::Future: Send,
-    ZV: Service<Arc<Block>, Response = block::Hash, Error = BoxError> + Send + Clone + 'static,
+    ZV: Service<zebra_consensus::Request, Response = block::Hash, Error = BoxError>
+        + Send
+        + Clone
+        + 'static,
     ZV::Future: Send,
     ZS: Service<zs::Request, Response = zs::Response, Error = BoxError> + Send + Clone + 'static,
     ZS::Future: Send,
@@ -338,7 +343,7 @@ where
             }
 
             verifier
-                .oneshot(block)
+                .oneshot(zebra_consensus::Request::Commit(block))
                 .await
                 .map(|hash| (hash, block_height))
         }
diff --git a/zebrad/src/components/inbound/tests/real_peer_set.rs b/zebrad/src/components/inbound/tests/real_peer_set.rs
index e1611fa90ff..c610f1a1f71 100644
--- a/zebrad/src/components/inbound/tests/real_peer_set.rs
+++ b/zebrad/src/components/inbound/tests/real_peer_set.rs
@@ -1,6 +1,6 @@
 //! Inbound service tests with a real peer set.
 
-use std::{iter, net::SocketAddr, sync::Arc};
+use std::{iter, net::SocketAddr};
 
 use futures::FutureExt;
 use indexmap::IndexSet;
@@ -13,7 +13,7 @@ use tower::{
 };
 
 use zebra_chain::{
-    block::{self, Block, Height},
+    block::{self, Height},
     parameters::Network,
     serialization::ZcashDeserializeInto,
     transaction::{AuthDigest, Hash as TxHash, Transaction, UnminedTx, UnminedTxId, WtxId},
@@ -603,7 +603,7 @@ async fn setup(
     Buffer<BoxService<mempool::Request, mempool::Response, BoxError>, mempool::Request>,
     Buffer<BoxService<zebra_state::Request, zebra_state::Response, BoxError>, zebra_state::Request>,
     // mocked services
-    MockService<Arc<Block>, block::Hash, PanicAssertion, VerifyChainError>,
+    MockService<zebra_consensus::Request, block::Hash, PanicAssertion, VerifyChainError>,
     MockService<transaction::Request, transaction::Response, PanicAssertion, TransactionError>,
     // real tasks
     JoinHandle<Result<(), BlockGossipError>>,
diff --git a/zebrad/src/components/sync.rs b/zebrad/src/components/sync.rs
index 1a502945bc1..33f42622559 100644
--- a/zebrad/src/components/sync.rs
+++ b/zebrad/src/components/sync.rs
@@ -2,7 +2,7 @@
 //!
 //! It is used when Zebra is a long way behind the current chain tip.
 
-use std::{cmp::max, collections::HashSet, pin::Pin, sync::Arc, task::Poll, time::Duration};
+use std::{cmp::max, collections::HashSet, pin::Pin, task::Poll, time::Duration};
 
 use color_eyre::eyre::{eyre, Report};
 use futures::stream::{FuturesUnordered, StreamExt};
@@ -15,7 +15,7 @@ use tower::{
 };
 
 use zebra_chain::{
-    block::{self, Block, Height},
+    block::{self, Height},
     chain_tip::ChainTip,
     parameters::genesis_hash,
 };
@@ -300,7 +300,7 @@ where
         + Clone
         + 'static,
     ZS::Future: Send,
-    ZV: Service<Arc<Block>, Response = block::Hash, Error = BoxError>
+    ZV: Service<zebra_consensus::Request, Response = block::Hash, Error = BoxError>
         + Send
         + Sync
         + Clone
@@ -381,7 +381,7 @@ where
         + Clone
         + 'static,
     ZS::Future: Send,
-    ZV: Service<Arc<Block>, Response = block::Hash, Error = BoxError>
+    ZV: Service<zebra_consensus::Request, Response = block::Hash, Error = BoxError>
         + Send
         + Sync
         + Clone
diff --git a/zebrad/src/components/sync/downloads.rs b/zebrad/src/components/sync/downloads.rs
index 10c4bda8f31..4b6b5f00256 100644
--- a/zebrad/src/components/sync/downloads.rs
+++ b/zebrad/src/components/sync/downloads.rs
@@ -24,7 +24,7 @@ use tower::{hedge, Service, ServiceExt};
 use tracing_futures::Instrument;
 
 use zebra_chain::{
-    block::{self, Block, Height},
+    block::{self, Height},
     chain_tip::ChainTip,
 };
 use zebra_network as zn;
@@ -163,7 +163,7 @@ pub struct Downloads<ZN, ZV, ZSTip>
 where
     ZN: Service<zn::Request, Response = zn::Response, Error = BoxError> + Send + Sync + 'static,
     ZN::Future: Send,
-    ZV: Service<Arc<Block>, Response = block::Hash, Error = BoxError>
+    ZV: Service<zebra_consensus::Request, Response = block::Hash, Error = BoxError>
         + Send
         + Sync
         + Clone
@@ -217,7 +217,7 @@ impl<ZN, ZV, ZSTip> Stream for Downloads<ZN, ZV, ZSTip>
 where
     ZN: Service<zn::Request, Response = zn::Response, Error = BoxError> + Send + Sync + 'static,
     ZN::Future: Send,
-    ZV: Service<Arc<Block>, Response = block::Hash, Error = BoxError>
+    ZV: Service<zebra_consensus::Request, Response = block::Hash, Error = BoxError>
         + Send
         + Sync
         + Clone
@@ -264,7 +264,7 @@ impl<ZN, ZV, ZSTip> Downloads<ZN, ZV, ZSTip>
 where
     ZN: Service<zn::Request, Response = zn::Response, Error = BoxError> + Send + Sync + 'static,
     ZN::Future: Send,
-    ZV: Service<Arc<Block>, Response = block::Hash, Error = BoxError>
+    ZV: Service<zebra_consensus::Request, Response = block::Hash, Error = BoxError>
         + Send
         + Sync
         + Clone
@@ -516,7 +516,7 @@ where
                 // Verify the block.
                 let mut rsp = verifier
                     .map_err(|error| BlockDownloadVerifyError::VerifierServiceError { error })?
-                    .call(block).boxed();
+                    .call(zebra_consensus::Request::Commit(block)).boxed();
 
                 // Add a shorter timeout to workaround a known bug (#5125)
                 let short_timeout_max = (max_checkpoint_height + FINAL_CHECKPOINT_BLOCK_VERIFY_TIMEOUT_LIMIT).expect("checkpoint block height is in valid range");
diff --git a/zebrad/src/components/sync/tests/vectors.rs b/zebrad/src/components/sync/tests/vectors.rs
index 4acc67760c7..468d74958ab 100644
--- a/zebrad/src/components/sync/tests/vectors.rs
+++ b/zebrad/src/components/sync/tests/vectors.rs
@@ -89,7 +89,7 @@ async fn sync_blocks_ok() -> Result<(), crate::BoxError> {
         .respond(zn::Response::Blocks(vec![Available(block0.clone())]));
 
     chain_verifier
-        .expect_request(block0)
+        .expect_request(zebra_consensus::Request::Commit(block0))
         .await
         .respond(block0_hash);
 
@@ -175,9 +175,9 @@ async fn sync_blocks_ok() -> Result<(), crate::BoxError> {
 
     for _ in 1..=2 {
         chain_verifier
-            .expect_request_that(|req| remaining_blocks.remove(&req.hash()).is_some())
+            .expect_request_that(|req| remaining_blocks.remove(&req.block().hash()).is_some())
             .await
-            .respond_with(|req| req.hash());
+            .respond_with(|req| req.block().hash());
     }
     assert_eq!(
         remaining_blocks,
@@ -239,9 +239,9 @@ async fn sync_blocks_ok() -> Result<(), crate::BoxError> {
 
     for _ in 3..=4 {
         chain_verifier
-            .expect_request_that(|req| remaining_blocks.remove(&req.hash()).is_some())
+            .expect_request_that(|req| remaining_blocks.remove(&req.block().hash()).is_some())
             .await
-            .respond_with(|req| req.hash());
+            .respond_with(|req| req.block().hash());
     }
     assert_eq!(
         remaining_blocks,
@@ -316,7 +316,7 @@ async fn sync_blocks_duplicate_hashes_ok() -> Result<(), crate::BoxError> {
         .respond(zn::Response::Blocks(vec![Available(block0.clone())]));
 
     chain_verifier
-        .expect_request(block0)
+        .expect_request(zebra_consensus::Request::Commit(block0))
         .await
         .respond(block0_hash);
 
@@ -404,9 +404,9 @@ async fn sync_blocks_duplicate_hashes_ok() -> Result<(), crate::BoxError> {
 
     for _ in 1..=2 {
         chain_verifier
-            .expect_request_that(|req| remaining_blocks.remove(&req.hash()).is_some())
+            .expect_request_that(|req| remaining_blocks.remove(&req.block().hash()).is_some())
             .await
-            .respond_with(|req| req.hash());
+            .respond_with(|req| req.block().hash());
     }
     assert_eq!(
         remaining_blocks,
@@ -470,9 +470,9 @@ async fn sync_blocks_duplicate_hashes_ok() -> Result<(), crate::BoxError> {
 
     for _ in 3..=4 {
         chain_verifier
-            .expect_request_that(|req| remaining_blocks.remove(&req.hash()).is_some())
+            .expect_request_that(|req| remaining_blocks.remove(&req.block().hash()).is_some())
             .await
-            .respond_with(|req| req.hash());
+            .respond_with(|req| req.block().hash());
     }
     assert_eq!(
         remaining_blocks,
@@ -598,7 +598,7 @@ async fn sync_block_too_high_obtain_tips() -> Result<(), crate::BoxError> {
         .respond(zn::Response::Blocks(vec![Available(block0.clone())]));
 
     chain_verifier
-        .expect_request(block0)
+        .expect_request(zebra_consensus::Request::Commit(block0))
         .await
         .respond(block0_hash);
 
@@ -759,7 +759,7 @@ async fn sync_block_too_high_extend_tips() -> Result<(), crate::BoxError> {
         .respond(zn::Response::Blocks(vec![Available(block0.clone())]));
 
     chain_verifier
-        .expect_request(block0)
+        .expect_request(zebra_consensus::Request::Commit(block0))
         .await
         .respond(block0_hash);
 
@@ -845,9 +845,9 @@ async fn sync_block_too_high_extend_tips() -> Result<(), crate::BoxError> {
 
     for _ in 1..=2 {
         chain_verifier
-            .expect_request_that(|req| remaining_blocks.remove(&req.hash()).is_some())
+            .expect_request_that(|req| remaining_blocks.remove(&req.block().hash()).is_some())
             .await
-            .respond_with(|req| req.hash());
+            .respond_with(|req| req.block().hash());
     }
     assert_eq!(
         remaining_blocks,
@@ -927,7 +927,7 @@ fn setup() -> (
     impl Future<Output = Result<(), Report>> + Send,
     SyncStatus,
     // ChainVerifier
-    MockService<Arc<Block>, block::Hash, PanicAssertion>,
+    MockService<zebra_consensus::Request, block::Hash, PanicAssertion>,
     // PeerSet
     MockService<zebra_network::Request, zebra_network::Response, PanicAssertion>,
     // StateService