diff --git a/cli/tests/unit/http_test.ts b/cli/tests/unit/http_test.ts
index b8eb3be842..f407c9186e 100644
--- a/cli/tests/unit/http_test.ts
+++ b/cli/tests/unit/http_test.ts
@@ -2762,6 +2762,39 @@ for (const compression of [true, false]) {
   });
 }
 
+Deno.test({
+  name: "request signal is aborted when response errors",
+  permissions: { net: true },
+  async fn() {
+    let httpConn: Deno.HttpConn;
+    const promise = (async () => {
+      const listener = Deno.listen({ port: 4501 });
+      const conn = await listener.accept();
+      listener.close();
+      httpConn = Deno.serveHttp(conn);
+      const ev = await httpConn.nextRequest();
+      const { request, respondWith } = ev!;
+
+      await delay(300);
+      await assertRejects(() => respondWith(new Response("Hello World")));
+      assert(request.signal.aborted);
+    })();
+
+    const abortController = new AbortController();
+
+    fetch("http://127.0.0.1:4501/", {
+      signal: abortController.signal,
+    }).catch(() => {
+      // ignore
+    });
+
+    await delay(100);
+    abortController.abort();
+    await promise;
+    httpConn!.close();
+  },
+});
+
 function chunkedBodyReader(h: Headers, r: BufReader): Deno.Reader {
   // Based on https://tools.ietf.org/html/rfc2616#section-19.4.6
   const tp = new TextProtoReader(r);
diff --git a/ext/http/01_http.js b/ext/http/01_http.js
index fee30f7f0e..7e648017bf 100644
--- a/ext/http/01_http.js
+++ b/ext/http/01_http.js
@@ -18,7 +18,7 @@ import {
   fromInnerRequest,
   newInnerRequest,
 } from "ext:deno_fetch/23_request.js";
-import * as abortSignal from "ext:deno_web/03_abort_signal.js";
+import { AbortController } from "ext:deno_web/03_abort_signal.js";
 import {
   _eventLoop,
   _idleTimeoutDuration,
@@ -135,10 +135,10 @@ class HttpConn {
       body !== null ? new InnerBody(body) : null,
       false,
     );
-    const signal = abortSignal.newSignal();
+    const abortController = new AbortController();
     const request = fromInnerRequest(
       innerRequest,
-      signal,
+      abortController.signal,
       "immutable",
       false,
     );
@@ -149,6 +149,7 @@ class HttpConn {
       request,
       this.#remoteAddr,
       this.#localAddr,
+      abortController,
     );
 
     return { request, respondWith };
@@ -185,6 +186,7 @@ function createRespondWith(
   request,
   remoteAddr,
   localAddr,
+  abortController,
 ) {
   return async function respondWith(resp) {
     try {
@@ -381,6 +383,9 @@ function createRespondWith(
         }
         ws[_serverHandleIdleTimeout]();
       }
+    } catch (error) {
+      abortController.abort(error);
+      throw error;
     } finally {
       if (SetPrototypeDelete(httpConn.managedResources, streamRid)) {
         core.close(streamRid);