diff --git a/src/apprt/gtk/App.zig b/src/apprt/gtk/App.zig
index f0ba41d3a..51249af69 100644
--- a/src/apprt/gtk/App.zig
+++ b/src/apprt/gtk/App.zig
@@ -70,9 +70,8 @@ x11_xkb: ?x11.Xkb = null,
 /// and initialization was successful.
 transient_cgroup_base: ?[]const u8 = null,
 
-/// True if we have initialized runtime CSS. We only need to do this once for the application, but
-/// we can't perform the intialization until we have created a window
-runtime_css_intialized: bool = false,
+/// CSS Provider for any styles based on ghostty configuration values
+css_provider: *c.GtkCssProvider,
 
 pub fn init(core_app: *CoreApp, opts: Options) !App {
     _ = opts;
@@ -272,6 +271,9 @@ pub fn init(core_app: *CoreApp, opts: Options) !App {
         );
     }
 
+    const css_provider = c.gtk_css_provider_new();
+    try loadRuntimeCss(&config, css_provider);
+
     return .{
         .core_app = core_app,
         .app = app,
@@ -284,6 +286,7 @@ pub fn init(core_app: *CoreApp, opts: Options) !App {
         // This means that another instance of the GTK app is running and
         // our "activate" call above will open a window.
         .running = c.g_application_get_is_remote(gapp) == 0,
+        .css_provider = css_provider,
     };
 }
 
@@ -331,6 +334,7 @@ pub fn reloadConfig(self: *App) !?*const Config {
 fn syncConfigChanges(self: *App) !void {
     try self.updateConfigErrors();
     try self.syncActionAccelerators();
+    try loadRuntimeCss(&self.config, self.css_provider);
 }
 
 /// This should be called whenever the configuration changes to update
@@ -383,6 +387,23 @@ fn syncActionAccelerator(
     );
 }
 
+fn loadRuntimeCss(config: *const Config, provider: *c.GtkCssProvider) !void {
+    const fill: Config.Color = config.@"unfocused-split-fill" orelse config.background;
+    var css_buf: [128]u8 = undefined;
+    const css = try std.fmt.bufPrintZ(
+        &css_buf,
+        "widget.unfocused-split {{ opacity: {d:.2}; }}\n.ghostty-surface>stack {{ background-color: rgb({d},{d},{d});}}",
+        .{
+            config.@"unfocused-split-opacity",
+            fill.r,
+            fill.g,
+            fill.b,
+        },
+    );
+    // Clears any previously loaded CSS from this provider
+    c.gtk_css_provider_load_from_string(provider, css);
+}
+
 /// Called by CoreApp to wake up the event loop.
 pub fn wakeup(self: App) void {
     _ = self;
diff --git a/src/apprt/gtk/Window.zig b/src/apprt/gtk/Window.zig
index b68d0370e..a151fe92a 100644
--- a/src/apprt/gtk/Window.zig
+++ b/src/apprt/gtk/Window.zig
@@ -72,34 +72,10 @@ pub fn init(self: *Window, app: *App) !void {
         c.gtk_widget_set_opacity(@ptrCast(window), app.config.@"background-opacity");
     }
 
-    if (!app.runtime_css_intialized) {
-        // Intialize runtime CSS. This CSS requires ghostty configuration values so we don't set it
-        // in style.css. We also have to have a window in order to add a style_context to a display,
-        // so we intialize after creation of our first window
-        app.runtime_css_intialized = true;
-
-        const display = c.gdk_display_get_default();
-        const provider = c.gtk_css_provider_new();
-        defer c.g_object_unref(provider);
-        const fill: Color = app.config.@"unfocused-split-fill" orelse app.config.background;
-        var css_buf: [128]u8 = undefined;
-
-        // We will add the unfocused-split class in our focus callbacks. We unconditionally add the
-        // background-color to the notebook stack because it only comes into play if we have an
-        // unfocused split
-        const css = try std.fmt.bufPrintZ(
-            &css_buf,
-            "widget.unfocused-split {{ opacity: {d:.2}; }}\nstack {{ background-color: rgb({d},{d},{d});}}",
-            .{
-                app.config.@"unfocused-split-opacity",
-                fill.r,
-                fill.g,
-                fill.b,
-            },
-        );
-        c.gtk_css_provider_load_from_string(provider, css);
-        c.gtk_style_context_add_provider_for_display(display, @ptrCast(provider), c.GTK_STYLE_PROVIDER_PRIORITY_APPLICATION);
-    }
+    // Internally, GTK ensures that only one instance of this provider exists in the provider list
+    // for the display.
+    const display = c.gdk_display_get_default();
+    c.gtk_style_context_add_provider_for_display(display, @ptrCast(app.css_provider), c.GTK_STYLE_PROVIDER_PRIORITY_APPLICATION);
 
     // Use the new GTK4 header bar. We only create a header bar if we have
     // window decorations.
@@ -131,6 +107,7 @@ pub fn init(self: *Window, app: *App) !void {
 
     // Create a notebook to hold our tabs.
     const notebook_widget = c.gtk_notebook_new();
+    c.gtk_widget_add_css_class(notebook_widget, "ghostty-surface");
     const notebook: *c.GtkNotebook = @ptrCast(notebook_widget);
     self.notebook = notebook;
     const notebook_tab_pos: c_uint = switch (app.config.@"gtk-tabs-location") {