diff --git a/packages/stack/src/HttpProxy.integration.test.ts b/packages/stack/src/HttpProxy.integration.test.ts
index bec4715c09..8e6398d412 100644
--- a/packages/stack/src/HttpProxy.integration.test.ts
+++ b/packages/stack/src/HttpProxy.integration.test.ts
@@ -38,6 +38,7 @@ class HttpProxyTestError extends Data.TaggedError("HttpProxyTestError")<{
 }> {}
 
 const captureErrors = captureLogs(["Error"]);
+const captureWarnings = captureLogs(["Error", "Warn"]);
 
 /** Upstream that resets its first `drops` accepted connections without responding. */
 const droppingBackend = (drops: number) => {
@@ -581,11 +582,7 @@ it.live("retries a bodyless request once when the upstream drops the connection
     }),
   ).pipe(
     Effect.provide(
-      Layer.mergeAll(
-        NodeHttpClient.layerNodeHttp,
-        NodeServices.layer,
-        captureLogs(["Error", "Warn"])(logs),
-      ),
+      Layer.mergeAll(NodeHttpClient.layerNodeHttp, NodeServices.layer, captureWarnings(logs)),
     ),
   );
 });
@@ -617,50 +614,63 @@ it.live("does not replay a request with a body when the upstream drops the conne
   );
 });
 
+/**
+ * Keep-alive upstream that answers once per connection and resets any reused connection;
+ * connections after `answered` are dropped unanswered.
+ */
+const oneRequestPerConnectionBackend = (answered = Number.POSITIVE_INFINITY) => {
+  let connections = 0;
+  const sockets = new Set<Socket>();
+  const server = createTcpServer((socket) => {
+    connections += 1;
+    sockets.add(socket);
+    socket.on("error", () => {});
+    socket.on("close", () => sockets.delete(socket));
+    if (connections > answered) {
+      socket.destroy();
+      return;
+    }
+    let buffered = Buffer.alloc(0);
+    let bodyEnd: number | undefined;
+    let replied = false;
+    socket.on("data", (chunk: Buffer) => {
+      if (replied) {
+        socket.resetAndDestroy();
+        return;
+      }
+      buffered = Buffer.concat([buffered, chunk]);
+      if (bodyEnd === undefined) {
+        const headerEnd = buffered.indexOf("\r\n\r\n");
+        if (headerEnd === -1) return;
+        const contentLength = Number(
+          /content-length:\s*(\d+)/iu.exec(
+            buffered.subarray(0, headerEnd).toString("latin1"),
+          )?.[1] ?? 0,
+        );
+        bodyEnd = headerEnd + 4 + contentLength;
+      }
+      if (buffered.length < bodyEnd) return;
+      replied = true;
+      socket.write("HTTP/1.1 200 OK\r\nConnection: keep-alive\r\nContent-Length: 2\r\n\r\nok");
+    });
+  });
+  return {
+    connections: () => connections,
+    listen: listen(server, {
+      beforeClose: () => {
+        for (const socket of sockets) socket.destroy();
+      },
+    }),
+  };
+};
+
 it.live(
   "succeeds a second POST when a keep-alive backend only answers the first request per connection",
   () =>
     Effect.scoped(
       Effect.gen(function* () {
-        let connections = 0;
-        const sockets = new Set<Socket>();
-        // Keeps each connection open after answering, then resets it if a second request reuses it.
-        const backend = createTcpServer((socket) => {
-          connections += 1;
-          sockets.add(socket);
-          socket.on("error", () => {});
-          socket.on("close", () => sockets.delete(socket));
-          let buffered = Buffer.alloc(0);
-          let bodyEnd: number | undefined;
-          let answered = false;
-          socket.on("data", (chunk: Buffer) => {
-            if (answered) {
-              socket.resetAndDestroy();
-              return;
-            }
-            buffered = Buffer.concat([buffered, chunk]);
-            if (bodyEnd === undefined) {
-              const headerEnd = buffered.indexOf("\r\n\r\n");
-              if (headerEnd === -1) return;
-              const contentLength = Number(
-                /content-length:\s*(\d+)/iu.exec(
-                  buffered.subarray(0, headerEnd).toString("latin1"),
-                )?.[1] ?? 0,
-              );
-              bodyEnd = headerEnd + 4 + contentLength;
-            }
-            if (buffered.length < bodyEnd) return;
-            answered = true;
-            socket.write(
-              "HTTP/1.1 200 OK\r\nConnection: keep-alive\r\nContent-Length: 2\r\n\r\nok",
-            );
-          });
-        });
-        const address = yield* listen(backend, {
-          beforeClose: () => {
-            for (const socket of sockets) socket.destroy();
-          },
-        });
+        const backend = oneRequestPerConnectionBackend();
+        const address = yield* backend.listen;
         const proxy = yield* makeHttpProxy({ host: "127.0.0.1", port: 0 });
         yield* proxy.setRoutes([{ id: "mcp", prefix: "/", target: Effect.succeed(address) }]);
         const first = yield* request(proxy.port, "/mcp", new TextEncoder().encode("first-body"));
@@ -669,11 +679,149 @@ it.live(
         const second = yield* request(proxy.port, "/mcp", new TextEncoder().encode("second-body"));
         expect(second.status).toBe(200);
         expect(new TextDecoder().decode(second.body)).toBe("ok");
-        expect(connections).toBe(2);
+        expect(backend.connections()).toBe(2);
       }),
     ).pipe(Effect.provide(Layer.merge(NodeServices.layer, NodeHttpClient.layerNodeHttp))),
 );
 
+it.live(
+  "retries a GET once on a fresh connection when its pooled connection resets unanswered",
+  () => {
+    const logs: Array<string> = [];
+    return Effect.scoped(
+      Effect.gen(function* () {
+        const backend = oneRequestPerConnectionBackend();
+        const address = yield* backend.listen;
+        const proxy = yield* makeHttpProxy({ host: "127.0.0.1", port: 0 });
+        yield* proxy.setRoutes([{ id: "studio", prefix: "/", target: Effect.succeed(address) }]);
+        const first = yield* request(proxy.port, "/", new Uint8Array(), {}, "GET");
+        expect(first.status).toBe(200);
+        const second = yield* request(proxy.port, "/", new Uint8Array(), {}, "GET");
+        expect(second.status).toBe(200);
+        expect(new TextDecoder().decode(second.body)).toBe("ok");
+        expect(backend.connections()).toBe(2);
+        expect(logs).toHaveLength(1);
+        expect(logs[0]).toContain("Route studio GET upstream failed before responding, retrying");
+      }),
+    ).pipe(
+      Effect.provide(
+        Layer.mergeAll(NodeHttpClient.layerNodeHttp, NodeServices.layer, captureWarnings(logs)),
+      ),
+    );
+  },
+);
+
+it.live("returns a gateway error when the fresh retry after a pooled reset also fails", () => {
+  const logs: Array<string> = [];
+  return Effect.scoped(
+    Effect.gen(function* () {
+      const backend = oneRequestPerConnectionBackend(1);
+      const address = yield* backend.listen;
+      const proxy = yield* makeHttpProxy({ host: "127.0.0.1", port: 0 });
+      yield* proxy.setRoutes([{ id: "studio", prefix: "/", target: Effect.succeed(address) }]);
+      const first = yield* request(proxy.port, "/", new Uint8Array(), {}, "GET");
+      expect(first.status).toBe(200);
+      const second = yield* request(proxy.port, "/", new Uint8Array(), {}, "GET");
+      expect(second.status).toBe(502);
+      expect(backend.connections()).toBe(2);
+      expect(logs).toHaveLength(2);
+      expect(logs[0]).toContain("Route studio GET upstream failed before responding, retrying");
+      expect(logs[1]).toContain("Route studio request failed");
+    }),
+  ).pipe(
+    Effect.provide(
+      Layer.mergeAll(NodeHttpClient.layerNodeHttp, NodeServices.layer, captureWarnings(logs)),
+    ),
+  );
+});
+
+it.live("delivers a keyed POST once when the upstream resets after reading its body", () => {
+  const logs: Array<string> = [];
+  return Effect.scoped(
+    Effect.gen(function* () {
+      const bodies: Array<string> = [];
+      let connections = 0;
+      // Answers GETs on a keep-alive connection; resets after reading a POST body in full.
+      const backend = createTcpServer((socket) => {
+        connections += 1;
+        socket.on("error", () => {});
+        let buffered = Buffer.alloc(0);
+        socket.on("data", (chunk: Buffer) => {
+          buffered = Buffer.concat([buffered, chunk]);
+          const headerEnd = buffered.indexOf("\r\n\r\n");
+          if (headerEnd === -1) return;
+          const head = buffered.subarray(0, headerEnd).toString("latin1");
+          const bodyEnd = headerEnd + 4 + Number(/content-length:\s*(\d+)/iu.exec(head)?.[1] ?? 0);
+          if (buffered.length < bodyEnd) return;
+          const body = buffered.subarray(headerEnd + 4, bodyEnd).toString();
+          buffered = buffered.subarray(bodyEnd);
+          if (head.startsWith("GET ")) {
+            socket.write(
+              "HTTP/1.1 200 OK\r\nConnection: keep-alive\r\nContent-Length: 2\r\n\r\nok",
+            );
+            return;
+          }
+          bodies.push(body);
+          socket.resetAndDestroy();
+        });
+      });
+      const address = yield* listen(backend);
+      const proxy = yield* makeHttpProxy({ host: "127.0.0.1", port: 0 });
+      yield* proxy.setRoutes([{ id: "rest", prefix: "/", target: Effect.succeed(address) }]);
+      const pooled = yield* request(proxy.port, "/rest/v1/", new Uint8Array(), {}, "GET");
+      expect(pooled.status).toBe(200);
+      const post = yield* request(proxy.port, "/rest/v1/rpc", new TextEncoder().encode("insert"), {
+        "idempotency-key": "insert",
+      });
+      expect(post.status).toBe(502);
+      expect(bodies).toEqual(["insert"]);
+      expect(connections).toBe(2);
+      expect(logs).toHaveLength(1);
+      expect(logs[0]).toContain("Route rest request failed");
+    }),
+  ).pipe(
+    Effect.provide(
+      Layer.mergeAll(NodeHttpClient.layerNodeHttp, NodeServices.layer, captureWarnings(logs)),
+    ),
+  );
+});
+
+it.live("reuses pooled upstream connections across thousands of concurrent requests", () =>
+  Effect.scoped(
+    Effect.gen(function* () {
+      let connections = 0;
+      const backend = createServer((incoming, outgoing) => {
+        incoming.resume();
+        incoming.once("end", () => outgoing.end(incoming.url));
+      });
+      backend.on("connection", () => {
+        connections += 1;
+      });
+      const address = yield* listen(backend);
+      const proxy = yield* makeHttpProxy({ host: "127.0.0.1", port: 0 });
+      yield* proxy.setRoutes([{ id: "rest", prefix: "/", target: Effect.succeed(address) }]);
+      const responses = yield* Effect.forEach(
+        Array.from({ length: 3000 }, (_, index) => index),
+        (index) =>
+          request(proxy.port, `/rest/v1/items?id=eq.${index}`, new Uint8Array(), {}, "GET").pipe(
+            Effect.map((response) => ({
+              index,
+              status: response.status,
+              body: new TextDecoder().decode(response.body),
+            })),
+          ),
+        { concurrency: 16 },
+      );
+      expect(
+        responses.filter(
+          ({ index, status, body }) => status !== 200 || body !== `/rest/v1/items?id=eq.${index}`,
+        ),
+      ).toEqual([]);
+      expect(connections).toBeLessThan(100);
+    }),
+  ).pipe(Effect.provide(Layer.merge(NodeServices.layer, NodeHttpClient.layerNodeHttp))),
+);
+
 it.live(
   "does not replay a bodyless non-idempotent request when the upstream drops the connection",
   () => {
diff --git a/packages/stack/src/HttpProxy.ts b/packages/stack/src/HttpProxy.ts
index 4b4e5f0485..d2ae57d119 100644
--- a/packages/stack/src/HttpProxy.ts
+++ b/packages/stack/src/HttpProxy.ts
@@ -1,7 +1,8 @@
-import { Data, Effect, FiberSet, Ref, Schedule, Scope } from "effect";
+import { Data, Effect, FiberSet, Ref, Scope } from "effect";
 import { PortError } from "./Ports.ts";
 import type { BackendAddress, ProxyError } from "./Proxy.ts";
 import {
+  Agent,
   createServer,
   request as upstreamRequest,
   type IncomingMessage,
@@ -74,6 +75,10 @@ const hasBody = (request: IncomingMessage) =>
   request.headers["transfer-encoding"] !== undefined ||
   Number(request.headers["content-length"] ?? 0) > 0;
 
+// A write can commit before its connection resets, so only safe, bodyless requests are resent.
+const isReplayable = (request: IncomingMessage) =>
+  safeMethods.has(request.method ?? "GET") && !hasBody(request);
+
 const headersFor = (headers: IncomingMessage["headers"]) =>
   Object.fromEntries(
     Object.entries(headers).filter(
@@ -225,30 +230,24 @@ const connectInterruptibly = Effect.fn("HttpProxy.connect")((address: BackendAdd
   }),
 );
 
-// Mirrors nginx `proxy_next_upstream error`: a backend that drops a fresh connection before
-// answering gets one more attempt, but only when nothing sent to the client or upstream would
-// need replaying.
-const retryOnce = (request: IncomingMessage, response: ServerResponse, route: HttpRoute) =>
-  Schedule.recurs(1).pipe(
-    Schedule.setInputType<HttpProxyError | HttpProxyDisconnected>(),
-    Schedule.while(
-      ({ input }) =>
-        input._tag === "HttpProxyError" &&
-        input.responded === false &&
-        !response.destroyed &&
-        safeMethods.has(request.method ?? "GET") &&
-        !hasBody(request),
-    ),
-    Schedule.tap(({ input }) =>
-      Effect.logWarning(
-        `Route ${route.id} ${request.method ?? "GET"} upstream failed before responding, retrying`,
-        input,
-      ),
-    ),
-  );
+// Mirrors nginx `proxy_next_upstream error`: a backend that drops a connection before answering
+// gets one more attempt, but only when nothing sent to the client or upstream would need replaying.
+const isRetryable =
+  (request: IncomingMessage, response: ServerResponse) =>
+  (error: HttpProxyError | HttpProxyDisconnected) =>
+    error._tag === "HttpProxyError" &&
+    error.responded === false &&
+    !response.destroyed &&
+    isReplayable(request);
 
 const forward = Effect.fn("HttpProxy.forward")(
-  (request: IncomingMessage, response: ServerResponse, route: HttpRoute, backend: BackendAddress) =>
+  (
+    request: IncomingMessage,
+    response: ServerResponse,
+    route: HttpRoute,
+    backend: BackendAddress,
+    agent: Agent | false,
+  ) =>
     Effect.callback<void, HttpProxyError | HttpProxyDisconnected>((resume) => {
       let outgoing: ReturnType<typeof upstreamRequest> | undefined;
       let incoming: IncomingMessage | undefined;
@@ -287,9 +286,7 @@ const forward = Effect.fn("HttpProxy.forward")(
           host: "path" in backend ? undefined : backend.host,
           port: "path" in backend ? undefined : backend.port,
           socketPath: "path" in backend ? backend.path : undefined,
-          // A reused upstream connection can be reset by a just-woken backend, and a body
-          // cannot be replayed.
-          agent: false,
+          agent,
           method: request.method,
           path: pathFor(request, route),
           // Bun ends a streamed upstream response early when the request says Connection: close.
@@ -326,11 +323,16 @@ const forward = Effect.fn("HttpProxy.forward")(
 );
 
 const proxyRequest = Effect.fn("HttpProxy.proxyRequest")(
-  (request: IncomingMessage, response: ServerResponse, route: HttpRoute) =>
+  (request: IncomingMessage, response: ServerResponse, route: HttpRoute, agent: Agent) =>
     Effect.gen(function* () {
       const backend = yield* Effect.raceFirst(route.target, disconnected(request, response));
-      yield* forward(request, response, route, backend).pipe(
-        Effect.retry(retryOnce(request, response, route)),
+      yield* forward(request, response, route, backend, isReplayable(request) ? agent : false).pipe(
+        Effect.catchIf(isRetryable(request, response), (error) =>
+          Effect.logWarning(
+            `Route ${route.id} ${request.method ?? "GET"} upstream failed before responding, retrying`,
+            error,
+          ).pipe(Effect.andThen(forward(request, response, route, backend, false))),
+        ),
       );
     }),
 );
@@ -405,6 +407,12 @@ export const makeHttpProxy = (options: {
 }): Effect.Effect<HttpProxy, PortError, Scope.Scope> =>
   Effect.gen(function* () {
     const routes = yield* Ref.make<ReadonlyArray<HttpRoute>>([]);
+    // Sockets per upstream stay unbounded so long-lived streamed responses never queue requests.
+    // Idle sockets close before Node upstreams' default 5 s keep-alive timeout can race a reuse.
+    const agent = yield* Effect.acquireRelease(
+      Effect.sync(() => new Agent({ keepAlive: true, timeout: 4_000 })),
+      (value) => Effect.sync(() => value.destroy()),
+    );
     const runRequest = yield* FiberSet.makeRuntime();
     const sockets = new Set<Socket>();
     const server = createServer((request, response) => {
@@ -422,7 +430,7 @@ export const makeHttpProxy = (options: {
               response.statusCode = 404;
               response.end("Not Found");
             } else {
-              yield* proxyRequest(request, response, route).pipe(
+              yield* proxyRequest(request, response, route, agent).pipe(
                 Effect.tapError((cause) =>
                   cause._tag === "HttpProxyDisconnected"
                     ? Effect.void