diff --git a/lib/graphql/schema/input_object.rb b/lib/graphql/schema/input_object.rb
index 981223d714..e59be672c7 100644
--- a/lib/graphql/schema/input_object.rb
+++ b/lib/graphql/schema/input_object.rb
@@ -70,11 +70,10 @@ def self.authorized?(obj, value, ctx)
       end
 
       def self.one_of
-        if !@one_of
-          if (required_arg = all_argument_definitions.find { |arg| arg.type.non_null? })
-            raise ArgumentError, "`one_of` may not be used with required arguments -- add `required: false` to `argument #{required_arg.keyword.inspect}` to use `one_of`"
+        if !one_of?
+          if all_argument_definitions.any? { |arg| arg.type.non_null? }
+            raise ArgumentError, "`one_of` may not be used with required arguments -- add `required: false` to argument definitions to use `one_of`"
           end
-          @one_of = true
           directive(GraphQL::Schema::Directive::OneOf)
         end
       end
@@ -123,8 +122,13 @@ def to_kwargs
       class << self
         def argument(*args, **kwargs, &block)
           argument_defn = super(*args, **kwargs, &block)
-          if one_of? && argument_defn.type.non_null?
-            raise ArgumentError, "`one_of` may not be used with required arguments -- add `required: false` to `argument #{argument_defn.keyword.inspect}` to use `one_of`"
+          if one_of?
+            if argument_defn.type.non_null?
+              raise ArgumentError, "Argument '#{argument_defn.path}' must be nullable because it is part of a OneOf type, add `required: false`."
+            end
+            if argument_defn.default_value?
+              raise ArgumentError, "Argument '#{argument_defn.path}' cannot have a default value because it is part of a OneOf type, remove `default_value: ...`."
+            end
           end
           # Add a method access
           method_name = argument_defn.keyword
diff --git a/spec/graphql/schema/directive/one_of_spec.rb b/spec/graphql/schema/directive/one_of_spec.rb
new file mode 100644
index 0000000000..1e4b828bee
--- /dev/null
+++ b/spec/graphql/schema/directive/one_of_spec.rb
@@ -0,0 +1,78 @@
+# frozen_string_literal: true
+require "spec_helper"
+
+describe GraphQL::Schema::Directive::OneOf do
+  let(:schema) do
+    this = self
+    output_type = Class.new(GraphQL::Schema::Object) do
+      graphql_name "OneOfOutput"
+
+      field :string, GraphQL::Types::String
+      field :int, GraphQL::Types::Int
+    end
+
+    query_type = Class.new(GraphQL::Schema::Object) do
+        graphql_name "Query"
+
+        field :one_of_field, output_type, null: false do
+          argument :one_of_arg, this.one_of_input_object
+        end
+
+        def one_of_field(one_of_arg:)
+          one_of_arg
+        end
+      end
+
+    Class.new(GraphQL::Schema) do
+      query(query_type)
+    end
+  end
+
+  let(:one_of_input_object) do
+    Class.new(GraphQL::Schema::InputObject) do
+      graphql_name "OneOfInputObject"
+      directive GraphQL::Schema::Directive::OneOf
+
+      argument :int, GraphQL::Types::Int
+      argument :string, GraphQL::Types::String
+    end
+  end
+
+  describe "defining oneOf input objects" do
+    describe "with a non-null argument" do
+      let(:one_of_input_object) do
+        Class.new(GraphQL::Schema::InputObject) do
+          graphql_name "OneOfInputObject"
+          directive GraphQL::Schema::Directive::OneOf
+
+          argument :int, GraphQL::Types::Int, required: true # rubocop:disable GraphQL/DefaultRequiredTrue
+          argument :string, GraphQL::Types::String
+        end
+      end
+
+      it "raises an error" do
+        error = assert_raises(ArgumentError) { schema }
+        expected_message = "Argument 'OneOfInputObject.int' must be nullable because it is part of a OneOf type, add `required: false`."
+        assert_equal(expected_message, error.message)
+      end
+    end
+
+    describe "when an argument has a default" do
+      let(:one_of_input_object) do
+        Class.new(GraphQL::Schema::InputObject) do
+          graphql_name "OneOfInputObject"
+          directive GraphQL::Schema::Directive::OneOf
+
+          argument :int, GraphQL::Types::Int, default_value: 1, required: false
+          argument :string, GraphQL::Types::String, required: false
+        end
+      end
+
+      it "raises an error" do
+        error = assert_raises(ArgumentError) { schema }
+        expected_message = "Argument 'OneOfInputObject.int' cannot have a default value because it is part of a OneOf type, remove `default_value: ...`."
+        assert_equal(expected_message, error.message)
+      end
+    end
+  end
+end
diff --git a/spec/graphql/schema/input_object_spec.rb b/spec/graphql/schema/input_object_spec.rb
index 581c399ff0..9167ac0a0c 100644
--- a/spec/graphql/schema/input_object_spec.rb
+++ b/spec/graphql/schema/input_object_spec.rb
@@ -1183,21 +1183,23 @@ def f(a:)
     it "doesn't work without required: false" do
       err1 = assert_raises ArgumentError do
         Class.new(GraphQL::Schema::InputObject) do
+          graphql_name "OneOfThing"
           argument :arg_1, GraphQL::Types::Int
           one_of
         end
       end
 
-      assert_equal "`one_of` may not be used with required arguments -- add `required: false` to `argument :arg_1` to use `one_of`", err1.message
+      assert_equal "`one_of` may not be used with required arguments -- add `required: false` to argument definitions to use `one_of`", err1.message
 
       err2 = assert_raises ArgumentError do
         Class.new(GraphQL::Schema::InputObject) do
+          graphql_name "OneOfThing"
           one_of
           argument :arg_2, GraphQL::Types::Int
         end
       end
 
-      assert_equal "`one_of` may not be used with required arguments -- add `required: false` to `argument :arg_2` to use `one_of`", err2.message
+      assert_equal "Argument 'OneOfThing.arg2' must be nullable because it is part of a OneOf type, add `required: false`.", err2.message
     end
 
     it "allows queries with only one value" do