diff --git a/src/apprt/gtk/Surface.zig b/src/apprt/gtk/Surface.zig
index 056a3f40b..180f986ca 100644
--- a/src/apprt/gtk/Surface.zig
+++ b/src/apprt/gtk/Surface.zig
@@ -347,6 +347,11 @@ cursor: ?*c.GdkCursor = null,
 /// pass it to GTK.
 title_text: ?[:0]const u8 = null,
 
+/// Our current working directory. We use this value for setting tooltips in
+/// the headerbar subtitle if we have focus. When set, the text in this buf
+/// will be null-terminated because we need to pass it to GTK.
+pwd: ?[:0]const u8 = null,
+
 /// The timer used to delay title updates in order to prevent flickering.
 update_title_timer: ?c.guint = null,
 
@@ -628,6 +633,7 @@ fn realize(self: *Surface) !void {
 pub fn deinit(self: *Surface) void {
     self.init_config.deinit(self.app.core_app.alloc);
     if (self.title_text) |title| self.app.core_app.alloc.free(title);
+    if (self.pwd) |pwd| self.app.core_app.alloc.free(pwd);
 
     // We don't allocate anything if we aren't realized.
     if (!self.realized) return;
@@ -876,7 +882,7 @@ fn updateTitleLabels(self: *Surface) void {
             // I don't know a way around this yet. I've tried re-hiding the
             // cursor after setting the title but it doesn't work, I think
             // due to some gtk event loop things...
-            c.gtk_window_set_title(window.window, title.ptr);
+            window.setTitle(title);
         }
     }
 }
@@ -929,11 +935,27 @@ pub fn getTitle(self: *Surface) ?[:0]const u8 {
     return null;
 }
 
+/// Set the current working directory of the surface.
+///
+/// In addition, update the tab's tooltip text, and if we are the focused child,
+/// update the subtitle of the containing window.
 pub fn setPwd(self: *Surface, pwd: [:0]const u8) !void {
-    // If we have a tab and are the focused child, then we have to update the tab
     if (self.container.tab()) |tab| {
         tab.setTooltipText(pwd);
+
+        if (tab.focus_child == self) {
+            if (self.container.window()) |window| {
+                if (self.app.config.@"window-subtitle" == .@"working-directory") window.setSubtitle(pwd);
+            }
+        }
     }
+
+    const alloc = self.app.core_app.alloc;
+
+    // Failing to set the surface's current working directory is not a big
+    // deal since we just used our slice parameter which is the same value.
+    if (self.pwd) |old| alloc.free(old);
+    self.pwd = alloc.dupeZ(u8, pwd) catch null;
 }
 
 pub fn setMouseShape(
@@ -1896,6 +1918,12 @@ fn gtkFocusEnter(_: *c.GtkEventControllerFocus, ud: ?*anyopaque) callconv(.C) vo
         self.unfocused_widget = null;
     }
 
+    if (self.pwd) |pwd| {
+        if (self.container.window()) |window| {
+            if (self.app.config.@"window-subtitle" == .@"working-directory") window.setSubtitle(pwd);
+        }
+    }
+
     // Notify our surface
     self.core_surface.focusCallback(true) catch |err| {
         log.err("error in focus callback err={}", .{err});
diff --git a/src/apprt/gtk/Window.zig b/src/apprt/gtk/Window.zig
index 63ee57d95..c2c69e281 100644
--- a/src/apprt/gtk/Window.zig
+++ b/src/apprt/gtk/Window.zig
@@ -453,6 +453,22 @@ pub fn deinit(self: *Window) void {
     }
 }
 
+/// Set the title of the window.
+pub fn setTitle(self: *Window, title: [:0]const u8) void {
+    if ((comptime adwaita.versionAtLeast(1, 4, 0)) and adwaita.versionAtLeast(1, 4, 0) and adwaita.enabled(&self.app.config) and self.app.config.@"gtk-titlebar") {
+        if (self.header) |header| header.setTitle(title);
+    } else {
+        c.gtk_window_set_title(self.window, title);
+    }
+}
+
+/// Set the subtitle of the window if it has one.
+pub fn setSubtitle(self: *Window, subtitle: [:0]const u8) void {
+    if ((comptime adwaita.versionAtLeast(1, 4, 0)) and adwaita.versionAtLeast(1, 4, 0) and adwaita.enabled(&self.app.config) and self.app.config.@"gtk-titlebar") {
+        if (self.header) |header| header.setSubtitle(subtitle);
+    }
+}
+
 /// Add a new tab to this window.
 pub fn newTab(self: *Window, parent: ?*CoreSurface) !void {
     const alloc = self.app.core_app.alloc;
diff --git a/src/apprt/gtk/headerbar.zig b/src/apprt/gtk/headerbar.zig
index 5bb92aca2..97c48a4c2 100644
--- a/src/apprt/gtk/headerbar.zig
+++ b/src/apprt/gtk/headerbar.zig
@@ -14,14 +14,15 @@ pub const HeaderBar = union(enum) {
         if ((comptime adwaita.versionAtLeast(1, 4, 0)) and
             adwaita.enabled(&window.app.config))
         {
-            return initAdw();
+            return initAdw(window);
         }
 
         return initGtk();
     }
 
-    fn initAdw() HeaderBar {
+    fn initAdw(window: *Window) HeaderBar {
         const headerbar = c.adw_header_bar_new();
+        c.adw_header_bar_set_title_widget(@ptrCast(headerbar), @ptrCast(c.adw_window_title_new(c.gtk_window_get_title(window.window) orelse "Ghostty", null)));
         return .{ .adw = @ptrCast(headerbar) };
     }
 
@@ -70,4 +71,26 @@ pub const HeaderBar = union(enum) {
             ),
         }
     }
+
+    pub fn setTitle(self: HeaderBar, title: [:0]const u8) void {
+        switch (self) {
+            .adw => |headerbar| if (comptime adwaita.versionAtLeast(0, 0, 0)) {
+                const window_title: *c.AdwWindowTitle = @ptrCast(c.adw_header_bar_get_title_widget(@ptrCast(headerbar)));
+                c.adw_window_title_set_title(window_title, title);
+            },
+            // The title is owned by the window when not using Adwaita
+            .gtk => unreachable,
+        }
+    }
+
+    pub fn setSubtitle(self: HeaderBar, subtitle: [:0]const u8) void {
+        switch (self) {
+            .adw => |headerbar| if (comptime adwaita.versionAtLeast(0, 0, 0)) {
+                const window_title: *c.AdwWindowTitle = @ptrCast(c.adw_header_bar_get_title_widget(@ptrCast(headerbar)));
+                c.adw_window_title_set_subtitle(window_title, subtitle);
+            },
+            // There is no subtitle unless Adwaita is used
+            .gtk => unreachable,
+        }
+    }
 };
diff --git a/src/apprt/gtk/notebook_adw.zig b/src/apprt/gtk/notebook_adw.zig
index 85083a97e..48f005467 100644
--- a/src/apprt/gtk/notebook_adw.zig
+++ b/src/apprt/gtk/notebook_adw.zig
@@ -159,5 +159,5 @@ fn adwSelectPage(_: *c.GObject, _: *c.GParamSpec, ud: ?*anyopaque) void {
     const window: *Window = @ptrCast(@alignCast(ud.?));
     const page = c.adw_tab_view_get_selected_page(window.notebook.adw.tab_view) orelse return;
     const title = c.adw_tab_page_get_title(page);
-    c.gtk_window_set_title(window.window, title);
+    window.setTitle(std.mem.span(title));
 }
diff --git a/src/apprt/gtk/notebook_gtk.zig b/src/apprt/gtk/notebook_gtk.zig
index 6e8b016ba..a2c482500 100644
--- a/src/apprt/gtk/notebook_gtk.zig
+++ b/src/apprt/gtk/notebook_gtk.zig
@@ -259,7 +259,7 @@ fn gtkSwitchPage(_: *c.GtkNotebook, page: *c.GtkWidget, _: usize, ud: ?*anyopaqu
     const gtk_label_box = @as(*c.GtkWidget, @ptrCast(c.gtk_notebook_get_tab_label(self.notebook, page)));
     const gtk_label = @as(*c.GtkLabel, @ptrCast(c.gtk_widget_get_first_child(gtk_label_box)));
     const label_text = c.gtk_label_get_text(gtk_label);
-    c.gtk_window_set_title(window.window, label_text);
+    window.setTitle(std.mem.span(label_text));
 }
 
 fn gtkNotebookCreateWindow(
diff --git a/src/config/Config.zig b/src/config/Config.zig
index 6cd6ad75e..6d2c026fe 100644
--- a/src/config/Config.zig
+++ b/src/config/Config.zig
@@ -1118,6 +1118,15 @@ keybind: Keybinds = .{},
 /// required to be a fixed-width font.
 @"window-title-font-family": ?[:0]const u8 = null,
 
+/// The text that will be displayed in the subtitle of the window. Valid values:
+///
+///   * `false` - Disable the subtitle.
+///   * `working-directory` - Set the subtitle to the working directory of the
+///      surface.
+///
+/// This feature is only supported on GTK with Adwaita enabled.
+@"window-subtitle": WindowSubtitle = .false,
+
 /// The theme to use for the windows. Valid values:
 ///
 ///   * `auto` - Determine the theme based on the configured terminal
@@ -3968,6 +3977,11 @@ pub const WindowPaddingColor = enum {
     @"extend-always",
 };
 
+pub const WindowSubtitle = enum {
+    false,
+    @"working-directory",
+};
+
 /// Color represents a color using RGB.
 ///
 /// This is a packed struct so that the C API to read color values just