diff --git a/src/commands/serve.rs b/src/commands/serve.rs
index d36cc9fe6d81..8f04c697f071 100644
--- a/src/commands/serve.rs
+++ b/src/commands/serve.rs
@@ -748,40 +748,49 @@ impl ServeCommand {
             _shutdown_guard: Box::new(shutdown.clone().increment(false)),
         });
 
-        if debuggee_store.is_some() {
-            for server in servers {
-                Self::serve_on_listener(
-                    server,
-                    shutdown.clone(),
-                    sem_connections,
-                    handler.clone(),
-                    debuggee_store,
-                )
-                .await?;
-
-                // There can only be one socket with a debugger attached.
-                break;
-            }
+        // If any listener fails then a shutdown is requested to bring down all
+        // the other listeners as well, but the drain below still happens to
+        // gracefully finish in-flight requests. The first error seen is then
+        // returned at the end.
+        let result = if debuggee_store.is_some() {
+            debug_assert_eq!(servers.len(), 1);
+            let server = servers.into_iter().next().unwrap();
+            Self::serve_on_listener(
+                server,
+                shutdown.clone(),
+                sem_connections,
+                handler.clone(),
+                debuggee_store,
+            )
+            .await
         } else {
-            let mut listener_tasks = vec![];
+            let mut listener_tasks = tokio::task::JoinSet::new();
 
             for server in servers {
-                listener_tasks.push(tokio::task::spawn(Self::serve_on_listener(
+                listener_tasks.spawn(Self::serve_on_listener(
                     server,
                     shutdown.clone(),
                     sem_connections.clone(),
                     handler.clone(),
                     None,
-                )));
+                ));
             }
 
-            for task in listener_tasks {
-                task.await??;
+            let mut result = Ok(());
+            while let Some(task_result) = listener_tasks.join_next().await {
+                let task_result = task_result
+                    .map_err(wasmtime::Error::from)
+                    .and_then(|result| result);
+                if let Err(e) = task_result {
+                    eprintln!("listener error: {e:?}");
+                    shutdown.request_shutdown();
+                    if result.is_ok() {
+                        result = Err(e);
+                    }
+                }
             }
-        }
-
-        // Don't allow any further requests to get picked up.
-        handler.state().sem_requests.close();
+            result
+        };
 
         drop(handler);
 
@@ -798,7 +807,7 @@ impl ServeCommand {
             }
         }
 
-        Ok(())
+        result
     }
 
     async fn serve_on_listener(
@@ -830,11 +839,12 @@ impl ServeCommand {
             // concurrent requests can't be served. Otherwise though spawn a
             // task to handle this client.
             match &mut debuggee_store {
-                Some(store) => handle_client(stream, &handler, Some(store)).await,
+                Some(store) => handle_client(stream, &handler, &shutdown, Some(store)).await,
                 None => {
                     let handler = handler.clone();
+                    let shutdown = shutdown.clone();
                     tokio::task::spawn(async move {
-                        handle_client(stream, &handler, None).await;
+                        handle_client(stream, &handler, &shutdown, None).await;
                         drop(shutdown_guard);
                         drop(connection_permit);
                     });
@@ -1251,6 +1261,7 @@ type Request = hyper::Request<hyper::body::Incoming>;
 async fn handle_client(
     client: impl AsyncRead + AsyncWrite + Send + Sync + Unpin + 'static,
     handler: &ProxyHandler<HostHandlerState>,
+    shutdown: &GracefulShutdown,
     debuggee_store: Option<&mut Store<Host>>,
 ) {
     // Hyper's `service_fn` takes an `Fn` closure, so to bridge the need to
@@ -1259,26 +1270,24 @@ async fn handle_client(
     // `Send`.
     let lock = &debuggee_store.map(tokio::sync::Mutex::new);
 
-    if let Err(e) = http1::Builder::new()
-        .keep_alive(true)
-        .serve_connection(
-            TokioIo::new(client),
-            hyper::service::service_fn(move |req| async move {
-                let mut debuggee_store = match &lock {
-                    Some(store) => Some(store.lock().await),
-                    None => None,
-                };
-                let debuggee_store = debuggee_store.as_mut().map(|s| &mut ***s);
-                match handle_request(handler, debuggee_store, req).await {
-                    Ok(r) => Ok::<_, Infallible>(r),
-                    Err(e) => {
-                        eprintln!("error: {e:?}");
-                        let status = e
-                            .downcast_ref::<ErrorResponse>()
-                            .map(|e| e.status())
-                            .unwrap_or(StatusCode::INTERNAL_SERVER_ERROR);
-                        let error_html = format!(
-                            "\
+    let conn = http1::Builder::new().keep_alive(true).serve_connection(
+        TokioIo::new(client),
+        hyper::service::service_fn(move |req| async move {
+            let mut debuggee_store = match &lock {
+                Some(store) => Some(store.lock().await),
+                None => None,
+            };
+            let debuggee_store = debuggee_store.as_mut().map(|s| &mut ***s);
+            match handle_request(handler, debuggee_store, req).await {
+                Ok(r) => Ok::<_, Infallible>(r),
+                Err(e) => {
+                    eprintln!("error: {e:?}");
+                    let status = e
+                        .downcast_ref::<ErrorResponse>()
+                        .map(|e| e.status())
+                        .unwrap_or(StatusCode::INTERNAL_SERVER_ERROR);
+                    let error_html = format!(
+                        "\
 <!doctype html>
 <html>
 <head>
@@ -1292,22 +1301,32 @@ async fn handle_client(
     </center>
 </body>
 </html>"
-                        );
-                        Ok(Response::builder()
-                            .status(status)
-                            .header("Content-Type", "text/html; charset=UTF-8")
-                            .body(
-                                Full::new(bytes::Bytes::from(error_html))
-                                    .map_err(|_| unreachable!())
-                                    .boxed_unsync(),
-                            )
-                            .unwrap())
-                    }
+                    );
+                    Ok(Response::builder()
+                        .status(status)
+                        .header("Content-Type", "text/html; charset=UTF-8")
+                        .body(
+                            Full::new(bytes::Bytes::from(error_html))
+                                .map_err(|_| unreachable!())
+                                .boxed_unsync(),
+                        )
+                        .unwrap())
                 }
-            }),
-        )
-        .await
-    {
+            }
+        }),
+    );
+    let mut conn = std::pin::pin!(conn);
+
+    // Use hyper's built-in support for graceful shutdown whenever the server
+    // here gets a shutdown request.
+    let result = tokio::select! {
+        result = conn.as_mut() => result,
+        _ = shutdown.requested() => {
+            conn.as_mut().graceful_shutdown();
+            conn.await
+        }
+    };
+    if let Err(e) = result {
         eprintln!("error: {e:?}");
     }
 }