diff --git a/crates/auto_update/src/auto_update.rs b/crates/auto_update/src/auto_update.rs
index 4193e8185c..8f1a76c974 100644
--- a/crates/auto_update/src/auto_update.rs
+++ b/crates/auto_update/src/auto_update.rs
@@ -180,6 +180,7 @@ pub struct AutoUpdater {
     pending_poll: Option<Task<Option<()>>>,
     quit_subscription: Option<gpui::Subscription>,
     update_check_type: UpdateCheckType,
+    _wake_subscription: gpui::Subscription,
     dismissed_status: Option<AutoUpdateStatus>,
 }
 
@@ -441,6 +442,16 @@ impl AutoUpdater {
         })
         .detach();
 
+        // A download or check that was in flight when the machine went to sleep
+        // is almost certainly riding a TCP connection that silently died during
+        // suspend, so it would otherwise appear to stall indefinitely.
+        let wake_subscription = cx.on_system_wake({
+            let this = cx.entity().downgrade();
+            move |cx| {
+                this.update(cx, |this, cx| this.restart_after_wake(cx)).ok();
+            }
+        });
+
         Self {
             status: AutoUpdateStatus::Idle,
             current_version,
@@ -448,10 +459,27 @@ impl AutoUpdater {
             pending_poll: None,
             quit_subscription,
             update_check_type: UpdateCheckType::Automatic,
+            _wake_subscription: wake_subscription,
             dismissed_status: None,
         }
     }
 
+    fn restart_after_wake(&mut self, cx: &mut Context<Self>) {
+        // Only network phases can be safely restarted. `Installing` is a local
+        // operation (mounting a dmg, rsync, etc.) that must not be interrupted.
+        if !matches!(
+            self.status,
+            AutoUpdateStatus::Checking | AutoUpdateStatus::Downloading { .. }
+        ) {
+            return;
+        }
+
+        let check_type = self.update_check_type;
+        self.pending_poll.take();
+        self.status = AutoUpdateStatus::Idle;
+        self.poll(check_type, cx);
+    }
+
     pub fn start_polling(&self, cx: &mut Context<Self>) -> Task<Result<()>> {
         let poll_interval =
             ReleaseChannel::try_global(cx).map_or(POLL_INTERVAL, |channel| match channel {
diff --git a/crates/gpui/src/app.rs b/crates/gpui/src/app.rs
index 5e09d6905a..72833abe52 100644
--- a/crates/gpui/src/app.rs
+++ b/crates/gpui/src/app.rs
@@ -282,23 +282,6 @@ impl Application {
         self
     }
 
-    /// Invokes a handler when the system wakes from sleep.
-    pub fn on_system_wake<F>(&self, mut callback: F) -> &Self
-    where
-        F: 'static + FnMut(&mut App),
-    {
-        let this = Rc::downgrade(&self.0);
-        self.0
-            .borrow_mut()
-            .platform
-            .on_system_wake(Box::new(move || {
-                if let Some(app) = this.upgrade() {
-                    callback(&mut app.borrow_mut());
-                }
-            }));
-        self
-    }
-
     /// Returns a handle to the [`BackgroundExecutor`] associated with this app, which can be used to spawn futures in the background.
     pub fn background_executor(&self) -> BackgroundExecutor {
         self.0.borrow().background_executor.clone()
@@ -717,6 +700,7 @@ pub struct App {
     pub(crate) keystroke_interceptors: SubscriberSet<(), KeystrokeObserver>,
     pub(crate) keyboard_layout_observers: SubscriberSet<(), Handler>,
     pub(crate) thermal_state_observers: SubscriberSet<(), Handler>,
+    pub(crate) system_wake_observers: SubscriberSet<(), Handler>,
     pub(crate) release_listeners: SubscriberSet<EntityId, ReleaseListener>,
     pub(crate) global_observers: SubscriberSet<TypeId, Handler>,
     pub(crate) quit_observers: SubscriberSet<(), QuitHandler>,
@@ -845,6 +829,7 @@ impl App {
                 keystroke_interceptors: SubscriberSet::new(),
                 keyboard_layout_observers: SubscriberSet::new(),
                 thermal_state_observers: SubscriberSet::new(),
+                system_wake_observers: SubscriberSet::new(),
                 global_observers: SubscriberSet::new(),
                 quit_observers: SubscriberSet::new(),
                 restart_observers: SubscriberSet::new(),
@@ -903,6 +888,18 @@ impl App {
             }
         }));
 
+        platform.on_system_wake(Box::new({
+            let app = Rc::downgrade(&app);
+            move || {
+                if let Some(app) = app.upgrade() {
+                    let cx = &mut app.borrow_mut();
+                    cx.system_wake_observers
+                        .clone()
+                        .retain(&(), move |callback| (callback)(cx));
+                }
+            }
+        }));
+
         platform.on_quit(Box::new({
             let cx = Rc::downgrade(&app);
             move || {
@@ -1339,6 +1336,22 @@ impl App {
         subscription
     }
 
+    /// Invokes a handler when the system wakes from sleep.
+    pub fn on_system_wake<F>(&self, mut callback: F) -> Subscription
+    where
+        F: 'static + FnMut(&mut App),
+    {
+        let (subscription, activate) = self.system_wake_observers.insert(
+            (),
+            Box::new(move |cx| {
+                callback(cx);
+                true
+            }),
+        );
+        activate();
+        subscription
+    }
+
     /// Returns the appearance of the application's windows.
     pub fn window_appearance(&self) -> WindowAppearance {
         self.platform.window_appearance()