diff --git a/_release-content/migration-guides/windowplugin_exit_systems_moved_to_last.md b/_release-content/migration-guides/windowplugin_exit_systems_moved_to_last.md
new file mode 100644
index 0000000000000..c60375b84abef
--- /dev/null
+++ b/_release-content/migration-guides/windowplugin_exit_systems_moved_to_last.md
@@ -0,0 +1,8 @@
+---
+title: "`WindowPlugin` exit systems moved to `Last`"
+pull_requests: [23624]
+---
+
+`bevy::window::close_when_requested`, `bevy::window::exit_on_all_closed` and `bevy::window::exit_on_primary_closed` have all been moved into the `Last` schedule to prevent systems that run after `Update` and rely on windows existing from panicking on the last frame of the application.
+
+`exit_on_all_closed` and `exit_on_primary_closed` have also been added to a new `SystemSet`, `ExitSystems`.
diff --git a/crates/bevy_window/src/lib.rs b/crates/bevy_window/src/lib.rs
index 608b6fc2f5e23..ab47aac8387dc 100644
--- a/crates/bevy_window/src/lib.rs
+++ b/crates/bevy_window/src/lib.rs
@@ -46,6 +46,7 @@ pub mod prelude {
 
 use alloc::sync::Arc;
 use bevy_app::prelude::*;
+use bevy_ecs::schedule::IntoScheduleConfigs;
 use bevy_platform::sync::Mutex;
 
 impl Default for WindowPlugin {
@@ -87,14 +88,14 @@ pub struct WindowPlugin {
     /// surprise your users. It is recommended to leave this setting to
     /// either [`ExitCondition::OnAllClosed`] or [`ExitCondition::OnPrimaryClosed`].
     ///
-    /// [`ExitCondition::OnAllClosed`] will add [`exit_on_all_closed`] to [`Update`].
-    /// [`ExitCondition::OnPrimaryClosed`] will add [`exit_on_primary_closed`] to [`Update`].
+    /// [`ExitCondition::OnAllClosed`] will add [`exit_on_all_closed`] to [`Last`].
+    /// [`ExitCondition::OnPrimaryClosed`] will add [`exit_on_primary_closed`] to [`Last`].
     pub exit_condition: ExitCondition,
 
     /// Whether to close windows when they are requested to be closed (i.e.
     /// when the close button is pressed).
     ///
-    /// If true, this plugin will add [`close_when_requested`] to [`Update`].
+    /// If true, this plugin will add [`close_when_requested`] to [`Last`].
     /// If this system (or a replacement) is not running, the close button will have no effect.
     /// This may surprise your users. It is recommended to leave this setting as `true`.
     pub close_when_requested: bool,
@@ -137,17 +138,17 @@ impl Plugin for WindowPlugin {
 
         match self.exit_condition {
             ExitCondition::OnPrimaryClosed => {
-                app.add_systems(PostUpdate, exit_on_primary_closed);
+                app.add_systems(Last, exit_on_primary_closed.in_set(ExitSystems));
             }
             ExitCondition::OnAllClosed => {
-                app.add_systems(PostUpdate, exit_on_all_closed);
+                app.add_systems(Last, exit_on_all_closed.in_set(ExitSystems));
             }
             ExitCondition::DontExit => {}
         }
 
         if self.close_when_requested {
             // Need to run before `exit_on_*` systems
-            app.add_systems(Update, close_when_requested);
+            app.add_systems(Last, close_when_requested.before(ExitSystems));
         }
     }
 }
@@ -157,11 +158,11 @@ impl Plugin for WindowPlugin {
 pub enum ExitCondition {
     /// Close application when the primary window is closed
     ///
-    /// The plugin will add [`exit_on_primary_closed`] to [`PostUpdate`].
+    /// The plugin will add [`exit_on_primary_closed`] to [`Last`].
     OnPrimaryClosed,
     /// Close application when all windows are closed
     ///
-    /// The plugin will add [`exit_on_all_closed`] to [`PostUpdate`].
+    /// The plugin will add [`exit_on_all_closed`] to [`Last`].
     OnAllClosed,
     /// Keep application running headless even after closing all windows
     ///
diff --git a/crates/bevy_window/src/system.rs b/crates/bevy_window/src/system.rs
index 112770e6097f4..9426def046e05 100644
--- a/crates/bevy_window/src/system.rs
+++ b/crates/bevy_window/src/system.rs
@@ -3,6 +3,11 @@ use crate::{ClosingWindow, PrimaryWindow, Window, WindowCloseRequested};
 use bevy_app::AppExit;
 use bevy_ecs::prelude::*;
 
+/// A [`SystemSet`] for the system that exits the application.
+/// Which can be either [`exit_on_all_closed`] or [`exit_on_primary_closed`].
+#[derive(SystemSet, Debug, Clone, PartialEq, Eq, Hash)]
+pub struct ExitSystems;
+
 /// Exit the application when there are no open windows.
 ///
 /// This system is added by the [`WindowPlugin`] in the default configuration.
diff --git a/crates/bevy_winit/src/lib.rs b/crates/bevy_winit/src/lib.rs
index 2bd3456e96259..3dff3dc655686 100644
--- a/crates/bevy_winit/src/lib.rs
+++ b/crates/bevy_winit/src/lib.rs
@@ -16,7 +16,7 @@ extern crate alloc;
 
 use bevy_derive::Deref;
 use bevy_reflect::Reflect;
-use bevy_window::{RawHandleWrapperHolder, WindowEvent};
+use bevy_window::{ExitSystems, RawHandleWrapperHolder, WindowEvent};
 use core::cell::RefCell;
 use winit::{event_loop::EventLoop, window::WindowId};
 
@@ -140,7 +140,7 @@ impl Plugin for WinitPlugin {
                     // so we don't need to care about its ordering relative to `changed_windows`
                     changed_windows.ambiguous_with(exit_on_all_closed),
                     changed_cursor_options,
-                    despawn_windows,
+                    despawn_windows.after(ExitSystems),
                     check_keyboard_focus_lost,
                 )
                     .chain(),