diff --git a/toolkit/components/remote/nsDBusRemoteServer.cpp b/toolkit/components/remote/nsDBusRemoteServer.cpp
index 4ed053e3cc6c..0f4e32c79ede 100644
--- a/toolkit/components/remote/nsDBusRemoteServer.cpp
+++ b/toolkit/components/remote/nsDBusRemoteServer.cpp
@@ -47,11 +47,7 @@ bool nsDBusRemoteServer::HandleOpenURL(const gchar* aInterfaceName,
     return false;
   }
 
-  guint32 timestamp = gtk_get_current_event_time();
-  if (timestamp == GDK_CURRENT_TIME) {
-    timestamp = guint32(g_get_monotonic_time() / 1000);
-  }
-  HandleCommandLine(aParam, timestamp);
+  HandleCommandLine(aParam, gtk_get_current_event_time());
   return true;
 }
 
diff --git a/toolkit/xre/nsAppRunner.cpp b/toolkit/xre/nsAppRunner.cpp
index 9161237fd440..e186689f619f 100644
--- a/toolkit/xre/nsAppRunner.cpp
+++ b/toolkit/xre/nsAppRunner.cpp
@@ -4943,8 +4943,12 @@ int XREMain::XRE_mainStartup(bool* aExitFlag) {
       // Try to remote the entire command line. If this fails, start up
       // normally.
 #  ifdef MOZ_WIDGET_GTK
-      const auto& startupToken =
+      auto& startupToken =
           GdkIsWaylandDisplay() ? mXDGActivationToken : mDesktopStartupID;
+#    ifdef MOZ_X11
+      if (GdkIsX11Display() && startupToken.IsEmpty())
+        startupToken = SynthesizeStartupToken();
+#    endif /* MOZ_X11 */
 #  else
       const nsCString startupToken;
 #  endif
diff --git a/widget/gtk/WidgetUtilsGtk.cpp b/widget/gtk/WidgetUtilsGtk.cpp
index 8228a4530beb..26ba66b27402 100644
--- a/widget/gtk/WidgetUtilsGtk.cpp
+++ b/widget/gtk/WidgetUtilsGtk.cpp
@@ -28,6 +28,11 @@
 #include <dlfcn.h>
 #include <glib.h>
 
+#ifdef MOZ_X11
+#  include <X11/Xlib.h>
+#  include <X11/Xatom.h>
+#endif /* MOZ_X11 */
+
 #undef LOGW
 #ifdef MOZ_LOGGING
 #  include "mozilla/Logging.h"
@@ -498,4 +503,70 @@ bool IsCancelledGError(GError* aGError) {
   return g_error_matches(aGError, G_IO_ERROR, G_IO_ERROR_CANCELLED);
 }
 
+#if defined(MOZ_X11)
+static unsigned long GetWindowUserTime(GdkDisplay* aDisplay,
+                                       uintptr_t aWindow) {
+  Atom actualType;
+  int actualFormat;
+  unsigned long numberOfItems;
+  unsigned long bytesAfter;
+  unsigned char* property = nullptr;
+  unsigned long userTime = 0;
+
+  Display* xDisplay = GDK_DISPLAY_XDISPLAY(aDisplay);
+  Atom atom =
+      gdk_x11_get_xatom_by_name_for_display(aDisplay, "_NET_WM_USER_TIME");
+
+  if (XGetWindowProperty(xDisplay, aWindow, atom, 0, 1, false, XA_CARDINAL,
+                         &actualType, &actualFormat, &numberOfItems,
+                         &bytesAfter, &property) == Success &&
+      property) {
+    if (numberOfItems == 1) {
+      userTime = *((unsigned long*)property);
+    }
+    XFree(property);
+  }
+
+  return userTime;
+}
+
+void FindLatestUserTime(GdkDisplay* aDisplay, uintptr_t aWindow,
+                        unsigned long* aLatestTime) {
+  Window rootReturn;
+  Window parentReturn;
+  Window* children;
+  unsigned int numberOfChildren;
+  unsigned long userTime;
+
+  Display* xDisplay = GDK_DISPLAY_XDISPLAY(aDisplay);
+
+  if (XQueryTree(xDisplay, aWindow, &rootReturn, &parentReturn, &children,
+                 &numberOfChildren)) {
+    for (unsigned int i = 0; i < numberOfChildren; i++) {
+      userTime = GetWindowUserTime(aDisplay, children[i]);
+      if (userTime > *aLatestTime) {
+        *aLatestTime = userTime;
+      }
+      FindLatestUserTime(aDisplay, children[i], aLatestTime);
+    }
+
+    XFree(children);
+  }
+}
+
+// Assume we're started from user interaction and infer user time if its missing
+nsCString SynthesizeStartupToken() {
+  unsigned long latestUserTime = 0;
+  FindLatestUserTime(gdk_display_get_default(),
+                     GDK_WINDOW_XID(gdk_get_default_root_window()),
+                     &latestUserTime);
+
+  if (latestUserTime == 0) {
+    return nsCString();
+  }
+
+  return nsPrintfCString("%s_TIME%lu", g_get_host_name(), latestUserTime);
+}
+#endif
+
 }  // namespace mozilla::widget
diff --git a/widget/gtk/WidgetUtilsGtk.h b/widget/gtk/WidgetUtilsGtk.h
index ffd7425ae5cb..5cf6604b3c11 100644
--- a/widget/gtk/WidgetUtilsGtk.h
+++ b/widget/gtk/WidgetUtilsGtk.h
@@ -9,7 +9,6 @@
 #include "nsString.h"
 #include "nsTArray.h"
 #include "mozilla/MozPromise.h"
-
 #include <stdint.h>
 
 typedef struct _GdkDisplay GdkDisplay;
@@ -78,6 +77,13 @@ RefPtr<FocusRequestPromise> RequestWaylandFocusPromise();
 
 bool IsCancelledGError(GError* aGError);
 
+#if defined(MOZ_X11)
+// Used by startup notifications
+nsCString SynthesizeStartupToken();
+void FindLatestUserTime(GdkDisplay* aDisplay, uintptr_t aWindow,
+                        unsigned long* aLatestTime);
+#endif
+
 }  // namespace mozilla::widget
 
 #endif  // WidgetUtilsGtk_h__
diff --git a/widget/gtk/nsWindow.cpp b/widget/gtk/nsWindow.cpp
index 28c0cb2641e2..e3f3cf40f5e6 100644
--- a/widget/gtk/nsWindow.cpp
+++ b/widget/gtk/nsWindow.cpp
@@ -3102,6 +3102,18 @@ void nsWindow::SetFocus(Raise aRaise, mozilla::dom::CallerType aCallerType) {
             return t;
           }
         }
+#if defined(MOZ_X11)
+        // If it's X11 and there's a startup token, use GDK_CURRENT_TIME, so
+        // gtk_window_present_with_time will pull the timestamp from the startup
+        // token.
+        if (GdkIsX11Display()) {
+          nsGTKToolkit* toolkit = nsGTKToolkit::GetToolkit();
+          const auto& startupToken = toolkit->GetStartupToken();
+          if (!startupToken.IsEmpty()) {
+            return static_cast<uint32_t>(GDK_CURRENT_TIME);
+          }
+        }
+#endif
         return GetLastUserInputTime();
       }();