diff --git a/UI/Qt/BrowserWindow.cpp b/UI/Qt/BrowserWindow.cpp
index 81de511a44..fc29eb26da 100644
--- a/UI/Qt/BrowserWindow.cpp
+++ b/UI/Qt/BrowserWindow.cpp
@@ -180,7 +180,7 @@ bool FullscreenMode::eventFilter(QObject* obj, QEvent* event)
     ASSERT(is_api_fullscreen());
     if (event->type() == QEvent::MouseMove) {
         QMouseEvent* mouse_event = static_cast<QMouseEvent*>(event);
-        maybe_animate_show_exit_button(mouse_event->pos());
+        maybe_animate_show_exit_button(m_window->mapFromGlobal(mouse_event->globalPosition().toPoint()));
     }
 
     return QObject::eventFilter(obj, event);
@@ -189,10 +189,14 @@ bool FullscreenMode::eventFilter(QObject* obj, QEvent* event)
 ExitFullscreenButton::ExitFullscreenButton(QWidget* parent)
     : QPushButton("Exit fullscreen", parent)
 {
+#if defined(AK_OS_MACOS)
+    // The web content view is a native QRhiWidget on macOS, so this overlay must also be native to remain above it.
+    setAttribute(Qt::WA_NativeWindow);
+#endif
     setStyleSheet("background-color:rgb(55, 99, 129); color: white; padding: 10px; border-radius: 5px;");
     adjustSize();
     hide();
-    m_widget_animation = new QPropertyAnimation(this, "pos");
+    m_widget_animation = new QPropertyAnimation(this, "pos", this);
 }
 
 void ExitFullscreenButton::animate_show()
@@ -201,12 +205,13 @@ void ExitFullscreenButton::animate_show()
         return;
 
     show();
-    QScreen* current_screen = screen();
-    QRect screen_geometry = current_screen->geometry();
+    raise();
 
-    int const destination_x = (screen_geometry.width() - width()) / 2;
-    int const destination_y = static_cast<int>(static_cast<float>(screen_geometry.height()) * 0.05);
+    auto const container_size = screen() ? screen()->geometry().size() : (parentWidget() ? parentWidget()->size() : QSize {});
+    int const destination_x = (container_size.width() - width()) / 2;
+    int const destination_y = static_cast<int>(static_cast<float>(container_size.height()) * 0.05);
 
+    m_widget_animation->stop();
     m_widget_animation->setDuration(FullscreenMode::button_animation_time());
     m_widget_animation->setStartValue(QPoint(destination_x, -height()));
     m_widget_animation->setEndValue(QPoint(destination_x, destination_y));
diff --git a/UI/Qt/Tab.cpp b/UI/Qt/Tab.cpp
index 1751d48546..f7017f91d7 100644
--- a/UI/Qt/Tab.cpp
+++ b/UI/Qt/Tab.cpp
@@ -494,13 +494,11 @@ Tab::Tab(BrowserWindow* window, RefPtr<WebView::WebContentClient> parent_client,
     };
 
     view().on_fullscreen_window = [this]() {
-        m_toolbar_container->hide();
         m_window->fullscreen_mode().enter(this);
     };
 
     view().on_exit_fullscreen_window = [this]() {
         m_window->fullscreen_mode().exit(FullscreenMode::ExitInitiatedBy::WebContent);
-        m_toolbar_container->show();
     };
 
     view().on_audio_play_state_changed = [this](auto play_state) {
diff --git a/UI/Qt/TabBar.cpp b/UI/Qt/TabBar.cpp
index 879aa92fc9..5be0dd6c31 100644
--- a/UI/Qt/TabBar.cpp
+++ b/UI/Qt/TabBar.cpp
@@ -1319,6 +1319,7 @@ void TabWidget::set_tab_bar_visible(bool visible)
 
     m_tab_bar_visible = visible;
     update_tab_chrome_visibility();
+    update_tab_layout();
 }
 
 void TabWidget::set_window_controls_visible(bool visible)
@@ -1579,6 +1580,8 @@ bool TabWidget::cursor_is_over_vertical_tabs() const
 
 int TabWidget::vertical_tabs_layout_width() const
 {
+    if (!m_tab_bar_visible)
+        return 0;
     return m_vertical_tabs_expanded ? m_vertical_tabs_expanded_width : VERTICAL_TABS_COLLAPSED_WIDTH;
 }
 
@@ -1725,7 +1728,7 @@ void TabWidget::set_resize_handle_property(char const* property, bool enabled)
 void TabWidget::update_vertical_tabs_resize_handle()
 {
     auto is_vertical = m_tab_bar->tab_layout() != TabLayout::Horizontal;
-    auto show_resize_handle = is_vertical && m_vertical_tabs_expanded;
+    auto show_resize_handle = m_tab_bar_visible && is_vertical && m_vertical_tabs_expanded;
     m_vertical_tabs_resize_handle->setVisible(show_resize_handle);
     if (!show_resize_handle) {
         m_vertical_tabs_resize_handle->releaseMouse();
@@ -1873,6 +1876,7 @@ void TabWidget::update_tab_chrome_visibility()
     auto is_horizontal = tab_layout == TabLayout::Horizontal;
     auto show_top_row = m_tab_bar_visible && is_horizontal;
     m_tab_bar_row->setVisible(show_top_row);
+    m_toolbar_container->setVisible(m_tab_bar_visible);
     m_vertical_tab_bar_column->setVisible(m_tab_bar_visible && !is_horizontal);
     update_vertical_tabs_content_separator();
 
@@ -1906,7 +1910,7 @@ void TabWidget::update_chrome_style()
 
 void TabWidget::update_vertical_tabs_overlay_geometry()
 {
-    if (m_tab_bar->tab_layout() == TabLayout::Horizontal) {
+    if (!m_tab_bar_visible || m_tab_bar->tab_layout() == TabLayout::Horizontal) {
         m_vertical_tab_bar_column->hide();
         return;
     }