diff --git a/rust/connlib/tunnel/src/lib.rs b/rust/connlib/tunnel/src/lib.rs
index 43dd8b061..099983346 100644
--- a/rust/connlib/tunnel/src/lib.rs
+++ b/rust/connlib/tunnel/src/lib.rs
@@ -9,7 +9,7 @@ use connlib_shared::{
     CallbackErrorFacade, Callbacks, Error, Result,
 };
 use device_channel::Device;
-use futures_util::{future::BoxFuture, task::AtomicWaker, FutureExt};
+use futures_util::{task::AtomicWaker, FutureExt};
 use peer::PacketTransform;
 use peer_store::PeerStore;
 use snownet::{Node, Server};
@@ -19,6 +19,7 @@ use std::{
     fmt,
     hash::Hash,
     io,
+    pin::Pin,
     task::{ready, Context, Poll},
     time::{Duration, Instant},
 };
@@ -122,6 +123,11 @@ where
             Poll::Pending => {}
         }
 
+        // After any state change, check what the new timeout is and reset it if necessary.
+        if self.connections_state.poll_timeout(cx).is_ready() {
+            cx.waker().wake_by_ref()
+        }
+
         Poll::Pending
     }
 }
@@ -180,6 +186,11 @@ where
             }
         }
 
+        // After any state change, check what the new timeout is and reset it if necessary.
+        if self.connections_state.poll_timeout(cx).is_ready() {
+            cx.waker().wake_by_ref()
+        }
+
         Poll::Pending
     }
 }
@@ -229,7 +240,7 @@ where
 struct ConnectionState<TRole, TId> {
     pub node: Node<TRole, TId>,
     write_buf: Box<[u8; MAX_UDP_SIZE]>,
-    connection_pool_timeout: BoxFuture<'static, std::time::Instant>,
+    timeout: Option<Pin<Box<tokio::time::Sleep>>>,
     stats_timer: tokio::time::Interval,
     sockets: Sockets,
 }
@@ -242,9 +253,9 @@ where
         Ok(ConnectionState {
             node: Node::new(private_key, std::time::Instant::now()),
             write_buf: Box::new([0; MAX_UDP_SIZE]),
-            connection_pool_timeout: sleep_until(std::time::Instant::now()).boxed(),
             sockets: Sockets::new()?,
             stats_timer: tokio::time::interval(Duration::from_secs(60)),
+            timeout: None,
         })
     }
 
@@ -335,17 +346,6 @@ where
     }
 
     fn poll_next_event(&mut self, cx: &mut Context<'_>) -> Poll<Event<TId>> {
-        if let Poll::Ready(prev_timeout) = self.connection_pool_timeout.poll_unpin(cx) {
-            self.node.handle_timeout(prev_timeout);
-            if let Some(new_timeout) = self.node.poll_timeout() {
-                debug_assert_ne!(prev_timeout, new_timeout, "Timer busy loop!");
-
-                self.connection_pool_timeout = sleep_until(new_timeout).boxed();
-            }
-
-            cx.waker().wake_by_ref();
-        }
-
         if self.stats_timer.poll_tick(cx).is_ready() {
             let (node_stats, conn_stats) = self.node.stats();
 
@@ -386,6 +386,33 @@ where
 
         Poll::Pending
     }
+
+    fn poll_timeout(&mut self, cx: &mut Context<'_>) -> Poll<()> {
+        if let Some(timeout) = self.node.poll_timeout() {
+            let timeout = tokio::time::Instant::from_std(timeout);
+
+            match self.timeout.as_mut() {
+                Some(existing_timeout) if existing_timeout.deadline() != timeout => {
+                    existing_timeout.as_mut().reset(timeout)
+                }
+                Some(_) => {}
+                None => self.timeout = Some(Box::pin(tokio::time::sleep_until(timeout))),
+            }
+        }
+
+        if let Some(timeout) = self.timeout.as_mut() {
+            ready!(timeout.poll_unpin(cx));
+            self.node.handle_timeout(timeout.deadline().into());
+
+            return Poll::Ready(());
+        }
+
+        // Technically, we should set a waker here because we don't have a timer.
+        // But the only place where we set a timer is a few lines up.
+        // That is the same path that will re-poll it so there is no point in using a waker.
+        // We might want to consider making a `MaybeSleep` type that encapsulates a waker so we don't need to think about it as hard.
+        Poll::Pending
+    }
 }
 
 pub enum Event<TId> {
@@ -403,9 +430,3 @@ pub enum Event<TId> {
     SendPacket(IpPacket<'static>),
     StopPeer(TId),
 }
-
-async fn sleep_until(deadline: Instant) -> Instant {
-    tokio::time::sleep_until(deadline.into()).await;
-
-    deadline
-}