diff --git a/cli/tests/unit/http_test.ts b/cli/tests/unit/http_test.ts
index d661acbd17..ab43323bd4 100644
--- a/cli/tests/unit/http_test.ts
+++ b/cli/tests/unit/http_test.ts
@@ -228,3 +228,47 @@ unitTest(
     await promise;
   },
 );
+
+unitTest(
+  { perms: { net: true } },
+  async function httpServerCancelBodyOnResponseFailure() {
+    const promise = (async () => {
+      const listener = Deno.listen({ port: 4501 });
+      const conn = await listener.accept();
+      const httpConn = Deno.serveHttp(conn);
+      const event = await httpConn.nextRequest();
+      assert(event);
+      const { respondWith } = event;
+      let cancelReason = null;
+      const responseError = await assertThrowsAsync(
+        async () => {
+          let interval = 0;
+          await respondWith(
+            new Response(
+              new ReadableStream({
+                start(controller) {
+                  interval = setInterval(() => {
+                    const message = `data: ${Date.now()}\n\n`;
+                    controller.enqueue(new TextEncoder().encode(message));
+                  }, 200);
+                },
+                cancel(reason) {
+                  cancelReason = reason;
+                  clearInterval(interval);
+                },
+              }),
+            ),
+          );
+        },
+        Deno.errors.Http,
+      );
+      assertEquals(cancelReason, responseError);
+      httpConn.close();
+      listener.close();
+    })();
+
+    const resp = await fetch("http://127.0.0.1:4501/");
+    await resp.body!.cancel();
+    await promise;
+  },
+);
diff --git a/runtime/js/40_http.js b/runtime/js/40_http.js
index 67faf19cba..afc5635ac9 100644
--- a/runtime/js/40_http.js
+++ b/runtime/js/40_http.js
@@ -136,40 +136,51 @@
         respBody = new Uint8Array(0);
       }
 
-      const responseBodyRid = await Deno.core.opAsync("op_http_response", [
-        responseSenderRid,
-        innerResp.status ?? 200,
-        innerResp.headerList,
-      ], respBody instanceof Uint8Array ? respBody : null);
+      let responseBodyRid;
+      try {
+        responseBodyRid = await Deno.core.opAsync("op_http_response", [
+          responseSenderRid,
+          innerResp.status ?? 200,
+          innerResp.headerList,
+        ], respBody instanceof Uint8Array ? respBody : null);
+      } catch (error) {
+        if (respBody !== null && respBody instanceof ReadableStream) {
+          await respBody.cancel(error);
+        }
+        throw error;
+      }
 
       // If `respond` returns a responseBodyRid, we should stream the body
       // to that resource.
       if (responseBodyRid !== null) {
-        if (respBody === null || !(respBody instanceof ReadableStream)) {
-          throw new TypeError("Unreachable");
-        }
-        const reader = respBody.getReader();
-        while (true) {
-          const { value, done } = await reader.read();
-          if (done) break;
-          if (!(value instanceof Uint8Array)) {
-            await reader.cancel("value not a Uint8Array");
-            break;
+        try {
+          if (respBody === null || !(respBody instanceof ReadableStream)) {
+            throw new TypeError("Unreachable");
           }
-          try {
-            await Deno.core.opAsync(
-              "op_http_response_write",
-              responseBodyRid,
-              value,
-            );
-          } catch (err) {
-            await reader.cancel(err);
-            break;
+          const reader = respBody.getReader();
+          while (true) {
+            const { value, done } = await reader.read();
+            if (done) break;
+            if (!(value instanceof Uint8Array)) {
+              await reader.cancel(new TypeError("Value not a Uint8Array"));
+              break;
+            }
+            try {
+              await Deno.core.opAsync(
+                "op_http_response_write",
+                responseBodyRid,
+                value,
+              );
+            } catch (error) {
+              await reader.cancel(error);
+              throw error;
+            }
           }
+        } finally {
+          // Once all chunks are sent, and the request body is closed, we can
+          // close the response body.
+          await Deno.core.opAsync("op_http_response_close", responseBodyRid);
         }
-        // Once all chunks are sent, and the request body is closed, we can close
-        // the response body.
-        await Deno.core.opAsync("op_http_response_close", responseBodyRid);
       }
     };
   }