diff --git a/rust/connlib/tunnel/src/io.rs b/rust/connlib/tunnel/src/io.rs
index cc22d70c4..96a7360fb 100644
--- a/rust/connlib/tunnel/src/io.rs
+++ b/rust/connlib/tunnel/src/io.rs
@@ -153,14 +153,21 @@ impl Io {
 
         if let Some(timeout) = self.timeout.as_mut() {
             if timeout.poll_unpin(cx).is_ready() {
-                let deadline = timeout.deadline().into();
+                // Always emit `now` as the timeout value.
+                // This ensures that time within our state machine is always monotonic.
+                // If we were to use the `deadline` of the timer instead, time may go backwards.
+                // That is because it is valid to set a `Sleep` to a timestamp in the past.
+                // It will resolve immediately but it will still report the old timestamp as its deadline.
+                // To guard against this case, specifically call `Instant::now` here.
+                let now = Instant::now();
+
                 self.timeout = None; // Clear the timeout.
 
                 // Piggy back onto the timeout we already have.
                 // It is not important when we call this, just needs to be called occasionally.
-                self.gso_queue.handle_timeout(deadline);
+                self.gso_queue.handle_timeout(now);
 
-                return Poll::Ready(Ok(Input::Timeout(deadline)));
+                return Poll::Ready(Ok(Input::Timeout(now)));
             }
         }
 
@@ -334,48 +341,85 @@ mod tests {
 
     #[tokio::test]
     async fn timer_is_reset_after_it_fires() {
-        let now = Instant::now();
+        let mut io = Io::for_test();
 
-        let mut io = Io::new(
-            Arc::new(|_| Err(io::Error::other("not implemented"))),
-            Arc::new(|_| Err(io::Error::other("not implemented"))),
-        );
-        io.set_tun(Box::new(DummyTun));
+        let deadline = Instant::now() + Duration::from_secs(1);
+        io.reset_timeout(deadline);
 
-        io.reset_timeout(now + Duration::from_secs(1));
-
-        let poll_fn = poll_fn(|cx| {
-            io.poll(
-                cx,
-                // SAFETY: This is a test and we never receive packets here.
-                unsafe { &mut *addr_of_mut!(DUMMY_BUF) },
-            )
-        })
-        .await
-        .unwrap();
-
-        let Input::Timeout(timeout) = poll_fn else {
+        let Input::Timeout(timeout) = io.next().await else {
             panic!("Unexpected result");
         };
 
-        assert_eq!(timeout, now + Duration::from_secs(1));
+        assert!(timeout >= deadline, "timer expire after deadline");
 
-        let poll = io.poll(
-            &mut Context::from_waker(noop_waker_ref()),
-            // SAFETY: This is a test and we never receive packets here.
-            unsafe { &mut *addr_of_mut!(DUMMY_BUF) },
-        );
+        let poll = io.poll_test();
 
         assert!(poll.is_pending());
         assert!(io.timeout.is_none());
     }
 
+    #[tokio::test]
+    async fn emits_now_in_case_timeout_is_in_the_past() {
+        let now = Instant::now();
+        let mut io = Io::for_test();
+
+        io.reset_timeout(now - Duration::from_secs(10));
+
+        let Input::Timeout(timeout) = io.next().await else {
+            panic!("Unexpected result");
+        };
+
+        assert!(timeout.duration_since(now) < Duration::from_millis(1));
+    }
+
     static mut DUMMY_BUF: Buffers = Buffers {
         ip: Vec::new(),
         udp4: Vec::new(),
         udp6: Vec::new(),
     };
 
+    /// Helper functions to make the test more concise.
+    impl Io {
+        fn for_test() -> Io {
+            let mut io = Io::new(
+                Arc::new(|_| Err(io::Error::other("not implemented"))),
+                Arc::new(|_| Err(io::Error::other("not implemented"))),
+            );
+            io.set_tun(Box::new(DummyTun));
+
+            io
+        }
+
+        async fn next(
+            &mut self,
+        ) -> Input<impl Iterator<Item = IpPacket>, impl Iterator<Item = DatagramIn<'static>>>
+        {
+            poll_fn(|cx| {
+                self.poll(
+                    cx,
+                    // SAFETY: This is a test and we never receive packets here.
+                    unsafe { &mut *addr_of_mut!(DUMMY_BUF) },
+                )
+            })
+            .await
+            .unwrap()
+        }
+
+        fn poll_test(
+            &mut self,
+        ) -> Poll<
+            io::Result<
+                Input<impl Iterator<Item = IpPacket>, impl Iterator<Item = DatagramIn<'static>>>,
+            >,
+        > {
+            self.poll(
+                &mut Context::from_waker(noop_waker_ref()),
+                // SAFETY: This is a test and we never receive packets here.
+                unsafe { &mut *addr_of_mut!(DUMMY_BUF) },
+            )
+        }
+    }
+
     struct DummyTun;
 
     impl Tun for DummyTun {