diff --git a/.changeset/proxyworker-per-request-fetch-failures.md b/.changeset/proxyworker-per-request-fetch-failures.md
new file mode 100644
index 00000000000..836e5edb72f
--- /dev/null
+++ b/.changeset/proxyworker-per-request-fetch-failures.md
@@ -0,0 +1,7 @@
+---
+"wrangler": patch
+---
+
+fix: do not exit `wrangler dev` when forwarding a single request to the Worker fails
+
+The dev proxy forwards every incoming request to the user Worker with `fetch()`. When that `fetch()` rejected — most commonly because the client disconnected while its request body was still being uploaded ("Network connection lost." / "Can't read from request stream because client disconnected"), or because a request the proxy had queued during startup or a reload was abandoned before it could be replayed — the rejection was reported as a fatal ProxyWorker error and the whole `wrangler dev` session exited. A rejected forward is the outcome of that one request, not a defect in the proxy, so it is now answered with a `502` and logged at debug level, and the dev session keeps running. Errors thrown while post-processing a response are still reported as before.
diff --git a/packages/wrangler/e2e/dev.test.ts b/packages/wrangler/e2e/dev.test.ts
index 1f785dc464e..654c4482120 100644
--- a/packages/wrangler/e2e/dev.test.ts
+++ b/packages/wrangler/e2e/dev.test.ts
@@ -3305,3 +3305,71 @@ describe(".env support in local dev", () => {
 		`);
 	});
 });
+
+describe("client disconnects", () => {
+	/**
+	 * Opens a POST with a large announced body, sends only the first chunk and
+	 * then destroys the connection — what a caller with a timeout does while
+	 * uploading. workerd then fails the read of that request body.
+	 */
+	function abortUploadMidBody(url: string): Promise<void> {
+		const { hostname, port } = new URL(url);
+		return new Promise((resolve, reject) => {
+			const socket = nodeNet.connect(Number(port), hostname, () => {
+				socket.write(
+					`POST /upload HTTP/1.1\r\nHost: ${hostname}:${port}\r\nContent-Type: application/octet-stream\r\nContent-Length: 2000000\r\n\r\n`
+				);
+				socket.write(Buffer.alloc(64 * 1024), () => {
+					socket.destroy();
+					resolve();
+				});
+			});
+			socket.on("error", reject);
+		});
+	}
+
+	it("does not exit `wrangler dev` when a client aborts a request mid-body", async ({
+		expect,
+	}) => {
+		const helper = new WranglerE2ETestHelper();
+		await helper.seed({
+			"wrangler.toml": dedent`
+				name = "${workerName}"
+				main = "src/index.ts"
+				compatibility_date = "2023-01-01"
+			`,
+			"src/index.ts": dedent`
+				export default {
+					async fetch(request) {
+						if (request.method === "POST") {
+							await request.text();
+						}
+						return new Response("ok");
+					}
+				}
+			`,
+			"package.json": dedent`
+				{
+					"name": "worker",
+					"version": "0.0.0",
+					"private": true
+				}
+			`,
+		});
+		const worker = helper.runLongLived("wrangler dev");
+		const { url } = await worker.waitForReady();
+		await expect(fetchText(url)).resolves.toBe("ok");
+
+		for (let i = 0; i < 3; i++) {
+			await abortUploadMidBody(url);
+			await setTimeout(500);
+		}
+
+		// The dev session must still be alive and serving.
+		await expect(
+			Promise.race([worker.exitCode, setTimeout(2_000, "still running")])
+		).resolves.toBe("still running");
+		expect(worker.currentOutput).not.toContain("Error inside ProxyWorker");
+		await expect(fetchText(url)).resolves.toBe("ok");
+	});
+});
diff --git a/packages/wrangler/templates/startDevWorker/ProxyWorker.ts b/packages/wrangler/templates/startDevWorker/ProxyWorker.ts
index 59b507d72fe..75671d667b0 100644
--- a/packages/wrangler/templates/startDevWorker/ProxyWorker.ts
+++ b/packages/wrangler/templates/startDevWorker/ProxyWorker.ts
@@ -165,6 +165,9 @@ export class ProxyWorker implements DurableObject {
 
 			// explicitly NOT await-ing this promise, we are in a loop and want to process the whole queue quickly + synchronously
 			void fetch(userWorkerUrl, new Request(request, { headers }))
+				.catch((error: Error) => {
+					throw new UserWorkerFetchError(error);
+				})
 				.then(async (res) => {
 					res = new Response(res.body, res);
 					rewriteUrlRelatedHeaders(res.headers, innerUrl, outerUrl);
@@ -197,6 +200,31 @@ export class ProxyWorker implements DurableObject {
 					if (
 						isSameUserWorkerOrigin(userWorkerUrl, this.proxyData?.userWorkerUrl)
 					) {
+						// The fetch itself rejected, so this request never reached a
+						// response: the UserWorker could not be reached, or the request
+						// body could not be read because the client that queued it (during
+						// startup or a reload) has since gone away. Either way it is the
+						// outcome of this one request, not a defect in the ProxyWorker, so
+						// answer it with a 502 instead of failing the whole dev session.
+						if (error instanceof UserWorkerFetchError) {
+							void sendMessageToProxyController(this.env, {
+								type: "debug-log",
+								args: [
+									"Could not proxy request to the UserWorker:",
+									request.method,
+									request.url,
+									error.message,
+								],
+							});
+							deferredResponse.resolve(
+								new Response(
+									`Could not proxy this request to your Worker: ${error.message}`,
+									{ status: 502 }
+								)
+							);
+							return;
+						}
+
 						void sendMessageToProxyController(this.env, {
 							type: "error",
 							error: {
@@ -284,6 +312,20 @@ function isRequestForLiveReloadWebsocket(req: Request): boolean {
 	return isWebSocketUpgrade && websocketProtocol === LIVE_RELOAD_PROTOCOL;
 }
 
+/**
+ * Marks a rejection of the `fetch()` to the UserWorker itself, as opposed to an
+ * error thrown while post-processing its response. A rejected fetch is a
+ * network-level outcome for a single request (UserWorker unreachable, or the
+ * client's request body could not be read because the client disconnected)
+ * and is never treated as a ProxyWorker failure.
+ */
+class UserWorkerFetchError extends Error {
+	constructor(cause: Error) {
+		super(cause.message, { cause });
+		this.name = "UserWorkerFetchError";
+	}
+}
+
 function sendMessageToProxyController(
 	env: Env,
 	message: ProxyWorkerOutgoingRequestBody