diff --git a/.changeset/big-waves-hammer.md b/.changeset/big-waves-hammer.md
new file mode 100644
index 000000000000..4682e09aa640
--- /dev/null
+++ b/.changeset/big-waves-hammer.md
@@ -0,0 +1,5 @@
+---
+"wrangler": patch
+---
+
+fix: debounce restarting worker on assets dir file changes when `--x-dev-env` is enabled.
diff --git a/packages/wrangler/e2e/dev.test.ts b/packages/wrangler/e2e/dev.test.ts
index 7ec1dc18ed57..4435c70b0c04 100644
--- a/packages/wrangler/e2e/dev.test.ts
+++ b/packages/wrangler/e2e/dev.test.ts
@@ -1452,6 +1452,53 @@ describe("watch mode", () => {
 			response = await fetch(`${url}/hey`);
 			expect(response.status).toBe(404);
 		});
+
+		it("debounces runtime restarts when assets are modified", async () => {
+			const helper = new WranglerE2ETestHelper();
+			await helper.seed({
+				"wrangler.toml": dedent`
+						name = "${workerName}"
+						compatibility_date = "2023-01-01"
+						main = "src/index.ts"
+
+						[assets]
+						directory = "./public"
+				`,
+				"src/index.ts": dedent`
+					export default {
+						async fetch(request) {
+							return new Response("Hello, World!")
+						}
+					}
+				`,
+				"public/index.html": "Hello from Assets",
+			});
+			const worker = helper.runLongLived("wrangler dev");
+
+			const { url } = await worker.waitForReady();
+
+			// Modify assets multiple times in quick succession
+
+			await helper.seed({
+				"public/a.html": "a",
+			});
+
+			await helper.seed({
+				"public/b.html": "b",
+			});
+
+			await helper.seed({
+				"public/c.html": "c",
+			});
+
+			await worker.waitForReload();
+
+			// The three changes should be debounced, so only one reload should occur
+			await expect(worker.waitForReload(5_000)).rejects.toThrowError();
+
+			// now check assets are still fetchable
+			await expect(fetchText(url)).resolves.toBe("Hello from Assets");
+		});
 	});
 
 	describe.each([
diff --git a/packages/wrangler/e2e/helpers/wrangler.ts b/packages/wrangler/e2e/helpers/wrangler.ts
index 3eb2a176589b..791add741de4 100644
--- a/packages/wrangler/e2e/helpers/wrangler.ts
+++ b/packages/wrangler/e2e/helpers/wrangler.ts
@@ -39,9 +39,10 @@ export class WranglerLongLivedCommand extends LongLivedCommand {
 		return match.groups as { url: string };
 	}
 
-	async waitForReload(): Promise<void> {
+	async waitForReload(readTimeout?: number): Promise<void> {
 		await this.readUntil(
-			/Detected changes, restarted server|Reloading local server\.\.\./
+			/Detected changes, restarted server|Reloading local server\.\.\./,
+			readTimeout
 		);
 	}
 }
diff --git a/packages/wrangler/src/api/startDevWorker/BundlerController.ts b/packages/wrangler/src/api/startDevWorker/BundlerController.ts
index c327ac9ebfbc..24688760f1ee 100644
--- a/packages/wrangler/src/api/startDevWorker/BundlerController.ts
+++ b/packages/wrangler/src/api/startDevWorker/BundlerController.ts
@@ -14,6 +14,7 @@ import { getAssetChangeMessage } from "../../dev";
 import { runBuild } from "../../dev/use-esbuild";
 import { logger } from "../../logger";
 import { isNavigatorDefined } from "../../navigator-user-agent";
+import { debounce } from "../../pages/utils";
 import { getWranglerTmpDir } from "../../paths";
 import { Controller } from "./BaseController";
 import { castErrorCause } from "./events";
@@ -264,6 +265,12 @@ export class BundlerController extends Controller<BundlerControllerEventMap> {
 	async #ensureWatchingAssets(config: StartDevWorkerOptions) {
 		await this.#assetsWatcher?.close();
 
+		const debouncedRefreshBundle = debounce(() => {
+			if (this.#currentBundle) {
+				this.emitBundleCompleteEvent(config, this.#currentBundle);
+			}
+		});
+
 		if (config.assets?.directory) {
 			this.#assetsWatcher = watch(config.assets.directory, {
 				persistent: true,
@@ -271,9 +278,7 @@ export class BundlerController extends Controller<BundlerControllerEventMap> {
 			}).on("all", async (eventName, filePath) => {
 				const message = getAssetChangeMessage(eventName, filePath);
 				logger.debug(`🌀 ${message}...`);
-				if (this.#currentBundle) {
-					this.emitBundleCompleteEvent(config, this.#currentBundle);
-				}
+				debouncedRefreshBundle();
 			});
 		}
 	}