diff --git a/cli/tests/unit/flash_test.ts b/cli/tests/unit/flash_test.ts
index 07be6dfcca..fef45beb9b 100644
--- a/cli/tests/unit/flash_test.ts
+++ b/cli/tests/unit/flash_test.ts
@@ -57,6 +57,35 @@ Deno.test(async function httpServerCanResolveHostnames() {
   await server;
 });
 
+Deno.test(async function httpServerRejectsOnAddrInUse() {
+  const ac = new AbortController();
+  const listeningPromise = deferred();
+
+  const server = Deno.serve({
+    handler: (_req) => new Response("ok"),
+    hostname: "localhost",
+    port: 4501,
+    signal: ac.signal,
+    onListen: onListen(listeningPromise),
+    onError: createOnErrorCb(ac),
+  });
+
+  assertRejects(
+    () =>
+      Deno.serve({
+        handler: (_req) => new Response("ok"),
+        hostname: "localhost",
+        port: 4501,
+        signal: ac.signal,
+        onListen: onListen(listeningPromise),
+        onError: createOnErrorCb(ac),
+      }),
+    Deno.errors.AddrInUse,
+  );
+  ac.abort();
+  await server;
+});
+
 Deno.test({ permissions: { net: true } }, async function httpServerBasic() {
   const ac = new AbortController();
   const promise = deferred();
diff --git a/ext/flash/01_http.js b/ext/flash/01_http.js
index 4867da1617..fbc24d73d2 100644
--- a/ext/flash/01_http.js
+++ b/ext/flash/01_http.js
@@ -28,7 +28,7 @@
   const {
     Function,
     ObjectPrototypeIsPrototypeOf,
-    PromiseResolve,
+    PromiseAll,
     TypedArrayPrototypeSubarray,
     TypeError,
     Uint8Array,
@@ -249,7 +249,8 @@
 
     core.opAsync("op_flash_wait_for_listening", serverId).then((port) => {
       onListen({ hostname: listenOpts.hostname, port });
-    });
+    }).catch(() => {});
+    const finishedPromise = serverPromise.catch(() => {});
 
     const server = {
       id: serverId,
@@ -257,7 +258,7 @@
       hostname: listenOpts.hostname,
       port: listenOpts.port,
       closed: false,
-      finished: PromiseResolve(serverPromise),
+      finished: finishedPromise,
       async close() {
         if (server.closed) {
           return;
@@ -551,7 +552,10 @@
       }, 1000);
     }
 
-    return await server.serve().catch(console.error);
+    await PromiseAll([
+      server.serve().catch(console.error),
+      serverPromise,
+    ]);
   }
 
   function createRequestBodyStream(serverId, token) {
diff --git a/ext/flash/lib.rs b/ext/flash/lib.rs
index 2c76c450fe..90363c0825 100644
--- a/ext/flash/lib.rs
+++ b/ext/flash/lib.rs
@@ -1313,8 +1313,11 @@ fn op_flash_wait_for_listening(
     server_ctx.listening_rx.take().unwrap()
   };
   Ok(async move {
-    let port = listening_rx.recv().await.unwrap();
-    Ok(port)
+    if let Some(port) = listening_rx.recv().await {
+      Ok(port)
+    } else {
+      Err(generic_error("This error will be discarded"))
+    }
   })
 }