diff --git a/templates/startDevWorker/ProxyWorker.ts b/templates/startDevWorker/ProxyWorker.ts
index fc28268c0080789eb143d5444167fd05a09521c1..38a1da13acce7f1ae9022acf93db8686f0410156 100644
--- a/templates/startDevWorker/ProxyWorker.ts
+++ b/templates/startDevWorker/ProxyWorker.ts
@@ -12,6 +12,7 @@ import type {
 
 interface Env {
 	PROXY_CONTROLLER: Fetcher;
+	LOCAL_HTTP: Fetcher;
 	PROXY_CONTROLLER_AUTH_SECRET: string;
 	DURABLE_OBJECT: DurableObjectNamespace;
 }
@@ -155,8 +156,15 @@ 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 }))
+			// Use Node's non-pooled HTTP transport only for ordinary local forwarding.
+			// Native fetch keeps remote previews and WebSocket upgrades unchanged.
+			const forwarded = new Request(request, { headers });
+			const response = userWorkerUrl.protocol === "http:" &&
+				["127.0.0.1", "localhost", "[::1]"].includes(userWorkerUrl.hostname) &&
+				!headers.has("Upgrade")
+				? this.env.LOCAL_HTTP.fetch(new Request(userWorkerUrl, forwarded))
+				: fetch(userWorkerUrl, forwarded);
+			void response
 				.then(async (res) => {
 					res = new Response(res.body, res);
 					rewriteUrlRelatedHeaders(res.headers, innerUrl, outerUrl);
@@ -187,7 +195,7 @@ export class ProxyWorker implements DurableObject {
 						this.proxyData && urlFromParts(this.proxyData.userWorkerUrl);
 
 					// only report errors if the downstream proxy has NOT changed
-					if (userWorkerUrl.href === newUserWorkerUrl?.href) {
+					if (userWorkerUrl.origin === newUserWorkerUrl?.origin) {
 						void sendMessageToProxyController(this.env, {
 							type: "error",
 							error: {
diff --git a/wrangler-dist/ProxyWorker.js b/wrangler-dist/ProxyWorker.js
index 274b5d17ed4fb22f33efafca76efaa9f85279fbd..b164e92c1327978d1fff6c4e35950299762bbc32 100644
--- a/wrangler-dist/ProxyWorker.js
+++ b/wrangler-dist/ProxyWorker.js
@@ -131,7 +131,12 @@ var ProxyWorker = class {
           headers.set(key, value);
         }
       }
-      void fetch(userWorkerUrl, new Request(request, { headers })).then(async (res) => {
+      // Keep remote/Upgrade requests native; local HTTP uses Node without pooling.
+      const forwarded = new Request(request, { headers });
+      const response = userWorkerUrl.protocol === "http:" && ["127.0.0.1", "localhost", "[::1]"].includes(userWorkerUrl.hostname) && !headers.has("Upgrade")
+        ? this.env.LOCAL_HTTP.fetch(new Request(userWorkerUrl, forwarded))
+        : fetch(userWorkerUrl, forwarded);
+      void response.then(async (res) => {
         res = new Response(res.body, res);
         rewriteUrlRelatedHeaders(res.headers, innerUrl, outerUrl);
         await checkForPreviewTokenError(res, this.env, proxyData);
@@ -146,7 +151,7 @@ var ProxyWorker = class {
         deferredResponse.resolve(res);
       }).catch((error) => {
         const newUserWorkerUrl = this.proxyData && urlFromParts(this.proxyData.userWorkerUrl);
-        if (userWorkerUrl.href === newUserWorkerUrl?.href) {
+        if (userWorkerUrl.origin === newUserWorkerUrl?.origin) {
           void sendMessageToProxyController(this.env, {
             type: "error",
             error: {
diff --git a/wrangler-dist/cli.js b/wrangler-dist/cli.js
index b47f45933ae3a366f425f426545f53213dcc9d2a..a2c2680e1de7203d7b5de193ff1e25095afc4125 100644
--- a/wrangler-dist/cli.js
+++ b/wrangler-dist/cli.js
@@ -213736,6 +213736,7 @@ var init_ProxyController = __esm({
       }
       ready = createDeferred();
       localServerReady = createDeferred();
+      localHttpDispatcher = new (require_undici().Agent)({ pipelining: 0 });
       proxyWorker;
       proxyWorkerOptions;
       inspectorProxyWorkerWebSocket;
@@ -213776,6 +213777,22 @@ var init_ProxyController = __esm({
               // However, the proxy worker only makes outgoing requests to the user Worker Miniflare instance, which _should_ receive CF-Connecting-IP
               stripCfConnectingIp: false,
               serviceBindings: {
+                // Avoid workerd's idle-close race without replaying non-idempotent requests.
+                LOCAL_HTTP: async (req) => {
+                  const headers = new (require_undici().Headers)(req.headers);
+                  headers.delete("connection");
+                  // Miniflare encodes loopback responses, so use fetch's decoded body.
+                  const response = await require_undici().fetch(req.url, {
+                    method: req.method,
+                    headers,
+                    body: req.body,
+                    signal: req.signal,
+                    duplex: "half",
+                    dispatcher: this.localHttpDispatcher,
+                    redirect: "manual"
+                  });
+                  return new miniflare.Response(response.body, response);
+                },
                 PROXY_CONTROLLER: /* @__PURE__ */ __name(async (req) => {
                   const message = await req.json();
                   this.onProxyWorkerMessage(message);
@@ -214144,6 +214161,7 @@ var init_ProxyController = __esm({
         const { proxyWorker } = this;
         this.proxyWorker = void 0;
         await Promise.all([
+          this.localHttpDispatcher.destroy(),
           proxyWorker?.dispose(),
           this.inspectorProxyWorkerWebSocket?.promise.then((ws) => ws.close()).catch(() => {
           })