diff --git a/Userland/Services/WindowServer/Animation.cpp b/Userland/Services/WindowServer/Animation.cpp
index 633331c1568..37067a9c43f 100644
--- a/Userland/Services/WindowServer/Animation.cpp
+++ b/Userland/Services/WindowServer/Animation.cpp
@@ -17,7 +17,8 @@ Animation::Animation()
 
 Animation::~Animation()
 {
-    Compositor::the().unregister_animation({}, *this);
+    if (!m_was_removed)
+        Compositor::the().unregister_animation({}, *this);
 }
 
 void Animation::set_duration(int duration_in_ms)
@@ -39,7 +40,12 @@ void Animation::stop()
         on_stop();
 }
 
-void Animation::update(Badge<Compositor>, Gfx::Painter& painter, Screen& screen, Gfx::DisjointRectSet& flush_rects)
+void Animation::was_removed(Badge<Compositor>)
+{
+    m_was_removed = true;
+}
+
+bool Animation::update(Badge<Compositor>, Gfx::Painter& painter, Screen& screen, Gfx::DisjointRectSet& flush_rects)
 {
     int elapsed_ms = m_timer.elapsed();
     float progress = min((float)elapsed_ms / (float)m_duration, 1.0f);
@@ -47,8 +53,7 @@ void Animation::update(Badge<Compositor>, Gfx::Painter& painter, Screen& screen,
     if (on_update)
         on_update(progress, painter, screen, flush_rects);
 
-    if (progress >= 1.0f)
-        stop();
+    return progress < 1.0f;
 }
 
 }
diff --git a/Userland/Services/WindowServer/Animation.h b/Userland/Services/WindowServer/Animation.h
index b8786d87342..89f5e7787d7 100644
--- a/Userland/Services/WindowServer/Animation.h
+++ b/Userland/Services/WindowServer/Animation.h
@@ -28,11 +28,12 @@ public:
 
     void start();
     void stop();
+    void was_removed(Badge<Compositor>);
 
     void set_duration(int duration_in_ms);
     int duration() const { return m_duration; }
 
-    void update(Badge<Compositor>, Gfx::Painter&, Screen&, Gfx::DisjointRectSet& flush_rects);
+    bool update(Badge<Compositor>, Gfx::Painter&, Screen&, Gfx::DisjointRectSet& flush_rects);
 
     Function<void(float progress, Gfx::Painter&, Screen&, Gfx::DisjointRectSet& flush_rects)> on_update;
     Function<void()> on_stop;
@@ -43,6 +44,7 @@ private:
     Core::ElapsedTimer m_timer;
     int m_duration { 0 };
     bool m_running { false };
+    bool m_was_removed { false };
 };
 
 }
diff --git a/Userland/Services/WindowServer/Compositor.cpp b/Userland/Services/WindowServer/Compositor.cpp
index a173a888ae2..2ca7f3ef52a 100644
--- a/Userland/Services/WindowServer/Compositor.cpp
+++ b/Userland/Services/WindowServer/Compositor.cpp
@@ -1460,9 +1460,25 @@ void Compositor::unregister_animation(Badge<Animation>, Animation& animation)
 void Compositor::update_animations(Screen& screen, Gfx::DisjointRectSet& flush_rects)
 {
     auto& painter = *screen.compositor_screen_data().m_back_painter;
-    for (RefPtr<Animation> animation : m_animations) {
-        animation->update({}, painter, screen, flush_rects);
-    }
+    // Iterating over the animations using remove_all_matching we can iterate
+    // and immediately remove finished animations without having to keep track
+    // of them in a separate container.
+    m_animations.remove_all_matching([&](auto* animation) {
+        if (!animation->update({}, painter, screen, flush_rects)) {
+            // Mark it as removed so that the Animation::on_stop handler doesn't
+            // trigger the Animation object from being destroyed, causing it to
+            // unregister while we still loop over them.
+            animation->was_removed({});
+
+            // Temporarily bump the ref count so that if the Animation::on_stop
+            // handler clears its own reference, it doesn't immediately destroy
+            // itself while we're still in the Function<> call
+            NonnullRefPtr<Animation> protect_animation(*animation);
+            animation->stop();
+            return true;
+        }
+        return false;
+    });
 }
 
 void Compositor::create_window_stack_switch_overlay(WindowStack& target_stack)