diff --git a/cli/tests/integration/watcher_tests.rs b/cli/tests/integration/watcher_tests.rs
index 58f7e11fa1..6e3319b11f 100644
--- a/cli/tests/integration/watcher_tests.rs
+++ b/cli/tests/integration/watcher_tests.rs
@@ -1167,3 +1167,68 @@ fn run_watch_dynamic_imports() {
 
   check_alive_then_kill(child);
 }
+
+// https://github.com/denoland/deno/issues/16267
+#[test]
+fn run_watch_flash() {
+  let filename = "watch_flash.js";
+  let t = TempDir::new();
+  let file_to_watch = t.path().join(filename);
+  write(
+    &file_to_watch,
+    r#"
+      console.log("Starting flash server...");
+      Deno.serve({
+        onListen() {
+            console.error("First server is listening");
+        },
+        handler: () => {},
+        port: 4601,
+      });
+    "#,
+  )
+  .unwrap();
+
+  let mut child = util::deno_cmd()
+    .current_dir(t.path())
+    .arg("run")
+    .arg("--watch")
+    .arg("--unstable")
+    .arg("--allow-net")
+    .arg("-L")
+    .arg("debug")
+    .arg(&file_to_watch)
+    .env("NO_COLOR", "1")
+    .stdout(std::process::Stdio::piped())
+    .stderr(std::process::Stdio::piped())
+    .spawn()
+    .unwrap();
+  let (mut stdout_lines, mut stderr_lines) = child_lines(&mut child);
+
+  wait_contains("Starting flash server...", &mut stdout_lines);
+  wait_for(
+    |m| m.contains("Watching paths") && m.contains(filename),
+    &mut stderr_lines,
+  );
+
+  write(
+    &file_to_watch,
+    r#"
+      console.log("Restarting flash server...");
+      Deno.serve({
+        onListen() {
+            console.error("Second server is listening");
+        },
+        handler: () => {},
+        port: 4601,
+      });
+    "#,
+  )
+  .unwrap();
+
+  wait_contains("File change detected! Restarting!", &mut stderr_lines);
+  wait_contains("Restarting flash server...", &mut stdout_lines);
+  wait_contains("Second server is listening", &mut stderr_lines);
+
+  check_alive_then_kill(child);
+}
diff --git a/cli/tests/unit/flash_test.ts b/cli/tests/unit/flash_test.ts
index 0240694553..c64a7fe5a9 100644
--- a/cli/tests/unit/flash_test.ts
+++ b/cli/tests/unit/flash_test.ts
@@ -70,6 +70,7 @@ Deno.test(async function httpServerRejectsOnAddrInUse() {
     onError: createOnErrorCb(ac),
   });
 
+  await listeningPromise;
   assertRejects(
     () =>
       Deno.serve({
diff --git a/ext/flash/01_http.js b/ext/flash/01_http.js
index 7a6b9bc47e..8eed6047e5 100644
--- a/ext/flash/01_http.js
+++ b/ext/flash/01_http.js
@@ -188,8 +188,8 @@
     return str;
   }
 
-  function prepareFastCalls() {
-    return core.ops.op_flash_make_request();
+  function prepareFastCalls(serverId) {
+    return core.ops.op_flash_make_request(serverId);
   }
 
   function hostnameForDisplay(hostname) {
@@ -482,15 +482,11 @@
 
       const serverId = opFn(listenOpts);
       const serverPromise = core.opAsync("op_flash_drive_server", serverId);
-
-      PromisePrototypeCatch(
-        PromisePrototypeThen(
-          core.opAsync("op_flash_wait_for_listening", serverId),
-          (port) => {
-            onListen({ hostname: listenOpts.hostname, port });
-          },
-        ),
-        () => {},
+      const listenPromise = PromisePrototypeThen(
+        core.opAsync("op_flash_wait_for_listening", serverId),
+        (port) => {
+          onListen({ hostname: listenOpts.hostname, port });
+        },
       );
       const finishedPromise = PromisePrototypeCatch(serverPromise, () => {});
 
@@ -506,7 +502,7 @@
             return;
           }
           server.closed = true;
-          await core.opAsync("op_flash_close_server", serverId);
+          core.ops.op_flash_close_server(serverId);
           await server.finished;
         },
         async serve() {
@@ -618,7 +614,7 @@
 
       signal?.addEventListener("abort", () => {
         clearInterval(dateInterval);
-        PromisePrototypeThen(server.close(), () => {}, () => {});
+        server.close();
       }, {
         once: true,
       });
@@ -633,7 +629,7 @@
         );
       }
 
-      const fastOp = prepareFastCalls();
+      const fastOp = prepareFastCalls(serverId);
       let nextRequestSync = () => fastOp.nextRequest();
       let getMethodSync = (token) => fastOp.getMethod(token);
       let respondFast = (token, response, shutdown) =>
@@ -653,8 +649,8 @@
       }
 
       await SafePromiseAll([
+        listenPromise,
         PromisePrototypeCatch(server.serve(), console.error),
-        serverPromise,
       ]);
     };
   }
diff --git a/ext/flash/lib.rs b/ext/flash/lib.rs
index b077b8d219..41d88b3a02 100644
--- a/ext/flash/lib.rs
+++ b/ext/flash/lib.rs
@@ -35,6 +35,7 @@ use mio::Events;
 use mio::Interest;
 use mio::Poll;
 use mio::Token;
+use mio::Waker;
 use serde::Deserialize;
 use serde::Serialize;
 use socket2::Socket;
@@ -55,7 +56,6 @@ use std::rc::Rc;
 use std::sync::Arc;
 use std::sync::Mutex;
 use std::task::Context;
-use std::time::Duration;
 use tokio::sync::mpsc;
 use tokio::task::JoinHandle;
 
@@ -76,15 +76,24 @@ pub struct FlashContext {
   pub servers: HashMap<u32, ServerContext>,
 }
 
+impl Drop for FlashContext {
+  fn drop(&mut self) {
+    // Signal each server instance to shutdown.
+    for (_, server) in self.servers.drain() {
+      let _ = server.waker.wake();
+    }
+  }
+}
+
 pub struct ServerContext {
   _addr: SocketAddr,
   tx: mpsc::Sender<Request>,
-  rx: mpsc::Receiver<Request>,
+  rx: Option<mpsc::Receiver<Request>>,
   requests: HashMap<u32, Request>,
   next_token: u32,
-  listening_rx: Option<mpsc::Receiver<u16>>,
-  close_tx: mpsc::Sender<()>,
+  listening_rx: Option<mpsc::Receiver<Result<u16, std::io::Error>>>,
   cancel_handle: Rc<CancelHandle>,
+  waker: Arc<Waker>,
 }
 
 #[derive(Debug, Eq, PartialEq)]
@@ -102,7 +111,10 @@ fn op_flash_respond(
   shutdown: bool,
 ) -> u32 {
   let flash_ctx = op_state.borrow_mut::<FlashContext>();
-  let ctx = flash_ctx.servers.get_mut(&server_id).unwrap();
+  let ctx = match flash_ctx.servers.get_mut(&server_id) {
+    Some(ctx) => ctx,
+    None => return 0,
+  };
   flash_respond(ctx, token, shutdown, &response)
 }
 
@@ -120,7 +132,10 @@ async fn op_flash_respond_async(
   let sock = {
     let mut op_state = state.borrow_mut();
     let flash_ctx = op_state.borrow_mut::<FlashContext>();
-    let ctx = flash_ctx.servers.get_mut(&server_id).unwrap();
+    let ctx = match flash_ctx.servers.get_mut(&server_id) {
+      Some(ctx) => ctx,
+      None => return Ok(()),
+    };
 
     match shutdown {
       true => {
@@ -384,15 +399,30 @@ fn op_flash_method(state: &mut OpState, server_id: u32, token: u32) -> u32 {
 }
 
 #[op]
-async fn op_flash_close_server(state: Rc<RefCell<OpState>>, server_id: u32) {
-  let close_tx = {
-    let mut op_state = state.borrow_mut();
-    let flash_ctx = op_state.borrow_mut::<FlashContext>();
-    let ctx = flash_ctx.servers.get_mut(&server_id).unwrap();
-    ctx.cancel_handle.cancel();
-    ctx.close_tx.clone()
+fn op_flash_drive_server(
+  state: &mut OpState,
+  server_id: u32,
+) -> Result<impl Future<Output = Result<(), AnyError>> + 'static, AnyError> {
+  let join_handle = {
+    let flash_ctx = state.borrow_mut::<FlashContext>();
+    flash_ctx
+      .join_handles
+      .remove(&server_id)
+      .ok_or_else(|| type_error("server not found"))?
   };
-  let _ = close_tx.send(()).await;
+  Ok(async move {
+    join_handle
+      .await
+      .map_err(|_| type_error("server join error"))??;
+    Ok(())
+  })
+}
+
+#[op]
+fn op_flash_close_server(state: &mut OpState, server_id: u32) {
+  let flash_ctx = state.borrow_mut::<FlashContext>();
+  let ctx = flash_ctx.servers.remove(&server_id).unwrap();
+  let _ = ctx.waker.wake();
 }
 
 #[op]
@@ -419,7 +449,7 @@ fn op_flash_path(
 fn next_request_sync(ctx: &mut ServerContext) -> u32 {
   let offset = ctx.next_token;
 
-  while let Ok(token) = ctx.rx.try_recv() {
+  while let Ok(token) = ctx.rx.as_mut().unwrap().try_recv() {
     ctx.requests.insert(ctx.next_token, token);
     ctx.next_token += 1;
   }
@@ -482,6 +512,7 @@ unsafe fn op_flash_get_method_fast(
 fn op_flash_make_request<'scope>(
   scope: &mut v8::HandleScope<'scope>,
   state: &mut OpState,
+  server_id: u32,
 ) -> serde_v8::Value<'scope> {
   let object_template = v8::ObjectTemplate::new(scope);
   assert!(object_template
@@ -489,7 +520,7 @@ fn op_flash_make_request<'scope>(
   let obj = object_template.new_instance(scope).unwrap();
   let ctx = {
     let flash_ctx = state.borrow_mut::<FlashContext>();
-    let ctx = flash_ctx.servers.get_mut(&0).unwrap();
+    let ctx = flash_ctx.servers.get_mut(&server_id).unwrap();
     ctx as *mut ServerContext
   };
   obj.set_aligned_pointer_in_internal_field(V8_WRAPPER_OBJECT_INDEX, ctx as _);
@@ -705,7 +736,10 @@ async fn op_flash_read_body(
     {
       let op_state = &mut state.borrow_mut();
       let flash_ctx = op_state.borrow_mut::<FlashContext>();
-      flash_ctx.servers.get_mut(&server_id).unwrap() as *mut ServerContext
+      match flash_ctx.servers.get_mut(&server_id) {
+        Some(ctx) => ctx as *mut ServerContext,
+        None => return 0,
+      }
     }
     .as_mut()
     .unwrap()
@@ -807,41 +841,40 @@ pub struct ListenOpts {
   reuseport: bool,
 }
 
+const SERVER_TOKEN: Token = Token(0);
+// Token reserved for the thread close signal.
+const WAKER_TOKEN: Token = Token(1);
+
+#[allow(clippy::too_many_arguments)]
 fn run_server(
   tx: mpsc::Sender<Request>,
-  listening_tx: mpsc::Sender<u16>,
-  mut close_rx: mpsc::Receiver<()>,
+  listening_tx: mpsc::Sender<Result<u16, std::io::Error>>,
   addr: SocketAddr,
   maybe_cert: Option<String>,
   maybe_key: Option<String>,
   reuseport: bool,
+  mut poll: Poll,
+  // We put a waker as an unused argument here as it needs to be alive both in
+  // the flash thread and in the main thread (otherwise the notification would
+  // not be caught by the event loop on Linux).
+  // See the comment in mio's example:
+  // https://docs.rs/mio/0.8.4/x86_64-unknown-linux-gnu/mio/struct.Waker.html#examples
+  _waker: Arc<Waker>,
 ) -> Result<(), AnyError> {
-  let domain = if addr.is_ipv4() {
-    socket2::Domain::IPV4
-  } else {
-    socket2::Domain::IPV6
+  let mut listener = match listen(addr, reuseport) {
+    Ok(listener) => listener,
+    Err(e) => {
+      listening_tx.blocking_send(Err(e)).unwrap();
+      return Err(generic_error(
+        "failed to start listening on the specified address",
+      ));
+    }
   };
-  let socket = Socket::new(domain, socket2::Type::STREAM, None)?;
 
-  #[cfg(not(windows))]
-  socket.set_reuse_address(true)?;
-  if reuseport {
-    #[cfg(target_os = "linux")]
-    socket.set_reuse_port(true)?;
-  }
-
-  let socket_addr = socket2::SockAddr::from(addr);
-  socket.bind(&socket_addr)?;
-  socket.listen(128)?;
-  socket.set_nonblocking(true)?;
-  let std_listener: std::net::TcpListener = socket.into();
-  let mut listener = TcpListener::from_std(std_listener);
-
-  let mut poll = Poll::new()?;
-  let token = Token(0);
+  // Register server.
   poll
     .registry()
-    .register(&mut listener, token, Interest::READABLE)
+    .register(&mut listener, SERVER_TOKEN, Interest::READABLE)
     .unwrap();
 
   let tls_context: Option<Arc<rustls::ServerConfig>> = {
@@ -863,30 +896,24 @@ fn run_server(
   };
 
   listening_tx
-    .blocking_send(listener.local_addr().unwrap().port())
+    .blocking_send(Ok(listener.local_addr().unwrap().port()))
     .unwrap();
   let mut sockets = HashMap::with_capacity(1000);
-  let mut counter: usize = 1;
+  let mut counter: usize = 2;
   let mut events = Events::with_capacity(1024);
   'outer: loop {
-    let result = close_rx.try_recv();
-    if result.is_ok() {
-      break 'outer;
-    }
-    // FIXME(bartlomieju): how does Tokio handle it? I just put random 100ms
-    // timeout here to handle close signal.
-    match poll.poll(&mut events, Some(Duration::from_millis(100))) {
+    match poll.poll(&mut events, None) {
       Err(ref e) if e.kind() == std::io::ErrorKind::Interrupted => continue,
       Err(e) => panic!("{}", e),
       Ok(()) => (),
     }
     'events: for event in &events {
-      if close_rx.try_recv().is_ok() {
-        break 'outer;
-      }
       let token = event.token();
       match token {
-        Token(0) => loop {
+        WAKER_TOKEN => {
+          break 'outer;
+        }
+        SERVER_TOKEN => loop {
           match listener.accept() {
             Ok((mut socket, _)) => {
               counter += 1;
@@ -1149,6 +1176,33 @@ fn run_server(
   Ok(())
 }
 
+#[inline]
+fn listen(
+  addr: SocketAddr,
+  reuseport: bool,
+) -> Result<TcpListener, std::io::Error> {
+  let domain = if addr.is_ipv4() {
+    socket2::Domain::IPV4
+  } else {
+    socket2::Domain::IPV6
+  };
+  let socket = Socket::new(domain, socket2::Type::STREAM, None)?;
+
+  #[cfg(not(windows))]
+  socket.set_reuse_address(true)?;
+  if reuseport {
+    #[cfg(target_os = "linux")]
+    socket.set_reuse_port(true)?;
+  }
+
+  let socket_addr = socket2::SockAddr::from(addr);
+  socket.bind(&socket_addr)?;
+  socket.listen(128)?;
+  socket.set_nonblocking(true)?;
+  let std_listener: std::net::TcpListener = socket.into();
+  Ok(TcpListener::from_std(std_listener))
+}
+
 fn make_addr_port_pair(hostname: &str, port: u16) -> (&str, u16) {
   // Default to localhost if given just the port. Example: ":80"
   if hostname.is_empty() {
@@ -1186,17 +1240,19 @@ where
     .next()
     .ok_or_else(|| generic_error("No resolved address found"))?;
   let (tx, rx) = mpsc::channel(100);
-  let (close_tx, close_rx) = mpsc::channel(1);
   let (listening_tx, listening_rx) = mpsc::channel(1);
+
+  let poll = Poll::new()?;
+  let waker = Arc::new(Waker::new(poll.registry(), WAKER_TOKEN).unwrap());
   let ctx = ServerContext {
     _addr: addr,
     tx,
-    rx,
+    rx: Some(rx),
     requests: HashMap::with_capacity(1000),
     next_token: 0,
-    close_tx,
     listening_rx: Some(listening_rx),
     cancel_handle: CancelHandle::new_rc(),
+    waker: waker.clone(),
   };
   let tx = ctx.tx.clone();
   let maybe_cert = opts.cert;
@@ -1206,11 +1262,12 @@ where
     run_server(
       tx,
       listening_tx,
-      close_rx,
       addr,
       maybe_cert,
       maybe_key,
       reuseport,
+      poll,
+      waker,
     )
   });
   let flash_ctx = state.borrow_mut::<FlashContext>();
@@ -1245,45 +1302,26 @@ where
 }
 
 #[op]
-fn op_flash_wait_for_listening(
-  state: &mut OpState,
+async fn op_flash_wait_for_listening(
+  state: Rc<RefCell<OpState>>,
   server_id: u32,
-) -> Result<impl Future<Output = Result<u16, AnyError>> + 'static, AnyError> {
+) -> Result<u16, AnyError> {
   let mut listening_rx = {
-    let flash_ctx = state.borrow_mut::<FlashContext>();
+    let mut op_state = state.borrow_mut();
+    let flash_ctx = op_state.borrow_mut::<FlashContext>();
     let server_ctx = flash_ctx
       .servers
       .get_mut(&server_id)
       .ok_or_else(|| type_error("server not found"))?;
     server_ctx.listening_rx.take().unwrap()
   };
-  Ok(async move {
-    if let Some(port) = listening_rx.recv().await {
-      Ok(port)
-    } else {
-      Err(generic_error("This error will be discarded"))
-    }
-  })
-}
-
-#[op]
-fn op_flash_drive_server(
-  state: &mut OpState,
-  server_id: u32,
-) -> Result<impl Future<Output = Result<(), AnyError>> + 'static, AnyError> {
-  let join_handle = {
-    let flash_ctx = state.borrow_mut::<FlashContext>();
-    flash_ctx
-      .join_handles
-      .remove(&server_id)
-      .ok_or_else(|| type_error("server not found"))?
-  };
-  Ok(async move {
-    join_handle
-      .await
-      .map_err(|_| type_error("server join error"))??;
-    Ok(())
-  })
+  match listening_rx.recv().await {
+    Some(Ok(port)) => Ok(port),
+    Some(Err(e)) => Err(e.into()),
+    _ => Err(generic_error(
+      "unknown error occurred while waiting for listening",
+    )),
+  }
 }
 
 // Asychronous version of op_flash_next. This can be a bottleneck under
@@ -1291,26 +1329,34 @@ fn op_flash_drive_server(
 // requests i.e `op_flash_next() == 0`.
 #[op]
 async fn op_flash_next_async(
-  op_state: Rc<RefCell<OpState>>,
+  state: Rc<RefCell<OpState>>,
   server_id: u32,
 ) -> u32 {
-  let ctx = {
-    let mut op_state = op_state.borrow_mut();
+  let mut op_state = state.borrow_mut();
+  let flash_ctx = op_state.borrow_mut::<FlashContext>();
+  let ctx = flash_ctx.servers.get_mut(&server_id).unwrap();
+  let cancel_handle = ctx.cancel_handle.clone();
+  let mut rx = ctx.rx.take().unwrap();
+  // We need to drop the borrow before await point.
+  drop(op_state);
+
+  if let Ok(Some(req)) = rx.recv().or_cancel(&cancel_handle).await {
+    let mut op_state = state.borrow_mut();
     let flash_ctx = op_state.borrow_mut::<FlashContext>();
     let ctx = flash_ctx.servers.get_mut(&server_id).unwrap();
-    ctx as *mut ServerContext
-  };
-  // SAFETY: we cannot hold op_state borrow across the await point. The JS caller
-  // is responsible for ensuring this is not called concurrently.
-  let ctx = unsafe { &mut *ctx };
-  let cancel_handle = &ctx.cancel_handle;
-
-  if let Ok(Some(req)) = ctx.rx.recv().or_cancel(cancel_handle).await {
     ctx.requests.insert(ctx.next_token, req);
     ctx.next_token += 1;
+    // Set the rx back.
+    ctx.rx = Some(rx);
     return 1;
   }
 
+  // Set the rx back.
+  let mut op_state = state.borrow_mut();
+  let flash_ctx = op_state.borrow_mut::<FlashContext>();
+  if let Some(ctx) = flash_ctx.servers.get_mut(&server_id) {
+    ctx.rx = Some(rx);
+  }
   0
 }
 
@@ -1478,11 +1524,11 @@ pub fn init<P: FlashPermissions + 'static>(unstable: bool) -> Extension {
       op_flash_next_async::decl(),
       op_flash_read_body::decl(),
       op_flash_upgrade_websocket::decl(),
-      op_flash_drive_server::decl(),
       op_flash_wait_for_listening::decl(),
       op_flash_first_packet::decl(),
       op_flash_has_body_stream::decl(),
       op_flash_close_server::decl(),
+      op_flash_drive_server::decl(),
       op_flash_make_request::decl(),
       op_flash_write_resource::decl(),
     ])