diff --git a/ports/servoshell/desktop/headed_window.rs b/ports/servoshell/desktop/headed_window.rs
index ee08b7c3ddb..203ca2c261d 100644
--- a/ports/servoshell/desktop/headed_window.rs
+++ b/ports/servoshell/desktop/headed_window.rs
@@ -62,6 +62,9 @@ pub struct Window {
     monitor: winit::monitor::MonitorHandle,
     webview_relative_mouse_point: Cell<Point2D<f32, DevicePixel>>,
     last_pressed: Cell<Option<(KeyboardEvent, Option<LogicalKey>)>>,
+    /// The inner size of the window in physical pixels which excludes OS decorations.
+    /// It equals viewport size + (0, toolbar height).
+    inner_size: Cell<PhysicalSize<u32>>,
     /// A map of winit's key codes to key values that are interpreted from
     /// winit's ReceivedChar events.
     keys_down: RefCell<HashMap<LogicalKey, Key>>,
@@ -73,7 +76,10 @@ pub struct Window {
     /// The `RenderingContext` of Servo itself. This is used to render Servo results
     /// temporarily until they can be blitted into the egui scene.
     rendering_context: Rc<OffscreenRenderingContext>,
-
+    /// The RenderingContext that renders directly onto the Window. This is used as
+    /// the target of egui rendering and also where Servo rendering results are finally
+    /// blitted.
+    window_rendering_context: Rc<WindowRenderingContext>,
     // Keep this as the last field of the struct to ensure that the rendering context is
     // dropped first.
     // (https://github.com/servo/servo/issues/36711)
@@ -158,12 +164,14 @@ impl Window {
             last_pressed: Cell::new(None),
             keys_down: RefCell::new(HashMap::new()),
             fullscreen: Cell::new(false),
+            inner_size: Cell::new(inner_size),
             monitor,
             screen_size,
             device_pixel_ratio_override: servoshell_preferences.device_pixel_ratio_override,
             xr_window_poses: RefCell::new(vec![]),
             modifiers_state: Cell::new(ModifiersState::empty()),
             toolbar_height: Cell::new(Default::default()),
+            window_rendering_context,
             rendering_context,
         }
     }
@@ -677,6 +685,13 @@ impl WindowPortsMethods for Window {
                     winit::window::Theme::Dark => Theme::Dark,
                 });
             },
+            WindowEvent::Resized(new_inner_size) => {
+                if self.inner_size.get() != new_inner_size {
+                    // This should always be set to inner size.
+                    // See https://github.com/servo/servo/issues/38369#issuecomment-3138378527
+                    self.window_rendering_context.resize(new_inner_size);
+                }
+            },
             WindowEvent::Ime(ime) => match ime {
                 Ime::Enabled => {
                     webview.notify_input_event(InputEvent::Ime(ImeEvent::Composition(
diff --git a/ports/servoshell/desktop/minibrowser.rs b/ports/servoshell/desktop/minibrowser.rs
index 1dd30539dfe..812fc711c0d 100644
--- a/ports/servoshell/desktop/minibrowser.rs
+++ b/ports/servoshell/desktop/minibrowser.rs
@@ -409,6 +409,9 @@ impl Minibrowser {
                 let rect = Box2D::from_origin_and_size(Point2D::origin(), size);
                 if rect != webview.rect() {
                     webview.move_resize(rect);
+                    // `rect` is sized to just the WebView viewport, which is required by
+                    // `OffscreenRenderingContext` See:
+                    // <https://github.com/servo/servo/issues/38369#issuecomment-3138378527>
                     webview.resize(PhysicalSize::new(size.width as u32, size.height as u32))
                 }