diff --git a/src/frontend-common/platform_misc_unix.cpp b/src/frontend-common/platform_misc_unix.cpp
index 0033b1ebc0..529752338e 100644
--- a/src/frontend-common/platform_misc_unix.cpp
+++ b/src/frontend-common/platform_misc_unix.cpp
@@ -41,63 +41,64 @@ static bool SetScreensaverInhibitX11(bool inhibit, const WindowInfo& wi)
 
 #elif defined(USE_DBUS)
 #include <dbus/dbus.h>
-bool ChangeScreenSaverStateDBus(const bool inhibit_requested, const char* program_name, const char* reason)
+static bool SetScreensaverInhibitorDBus(const bool inhibit_requested, const char* program_name, const char* reason)
 {
   static dbus_uint32_t s_cookie;
-  // "error_dbus" doesn't need to be cleared in the end with "dbus_message_unref" at least if there is
-  // no error set, since calling "dbus_error_free" reinitializes it like "dbus_error_init" after freeing.
+  const char* bus_method = (inhibit_requested) ? "Inhibit" : "UnInhibit";
   DBusError error_dbus;
-  dbus_error_init(&error_dbus);
   DBusConnection* connection = nullptr;
   DBusMessage* message = nullptr;
   DBusMessage* response = nullptr;
-  // Initialized here because initializations should be before "goto" statements.
-  const char* bus_method = (inhibit_requested) ? "Inhibit" : "UnInhibit";
-  // "dbus_bus_get" gets a pointer to the same connection in libdbus, if exists, without creating a new connection.
-  // this doesn't need to be deleted, except if there's an error then calling "dbus_connection_unref", to free it,
-  // might be better so a new connection is established on the next try.
+  DBusMessageIter message_itr;
+
+  dbus_error_init(&error_dbus);
+  // Calling dbus_bus_get() after the first time returns a pointer to the existing connection.
   if (!(connection = dbus_bus_get(DBUS_BUS_SESSION, &error_dbus)) || (dbus_error_is_set(&error_dbus)))
-    goto cleanup;
+    goto error_cleanup;
+  dbus_connection_set_exit_on_disconnect(connection, false);
   if (!(message = dbus_message_new_method_call("org.freedesktop.ScreenSaver", "/org/freedesktop/ScreenSaver",
                                                "org.freedesktop.ScreenSaver", bus_method)))
-    goto cleanup;
+    goto error_cleanup;
   // Initialize an append iterator for the message, gets freed with the message.
-  DBusMessageIter message_itr;
   dbus_message_iter_init_append(message, &message_itr);
   if (inhibit_requested)
   {
+    // Guard against repeat inhibitions which would add extra inhibitors each generating a different cookie.
+    if (s_cookie)
+      goto repeat_inhibit_cleanup;
     // Append process/window name.
     if (!dbus_message_iter_append_basic(&message_itr, DBUS_TYPE_STRING, &program_name))
-      goto cleanup;
+      goto error_cleanup;
     // Append reason for inhibiting the screensaver.
     if (!dbus_message_iter_append_basic(&message_itr, DBUS_TYPE_STRING, &reason))
-      goto cleanup;
+      goto error_cleanup;
   }
   else
   {
     // Only Append the cookie.
     if (!dbus_message_iter_append_basic(&message_itr, DBUS_TYPE_UINT32, &s_cookie))
-      goto cleanup;
+      goto error_cleanup;
   }
   // Send message and get response.
   if (!(response =
           dbus_connection_send_with_reply_and_block(connection, message, DBUS_TIMEOUT_USE_DEFAULT, &error_dbus)) ||
       dbus_error_is_set(&error_dbus))
-    goto cleanup;
+    goto error_cleanup;
+  s_cookie = 0;
   if (inhibit_requested)
   {
     // Get the cookie from the response message.
-    if (!dbus_message_get_args(response, &error_dbus, DBUS_TYPE_UINT32, &s_cookie, DBUS_TYPE_INVALID))
-      goto cleanup;
+    if (!dbus_message_get_args(response, &error_dbus, DBUS_TYPE_UINT32, &s_cookie, DBUS_TYPE_INVALID) ||
+        dbus_error_is_set(&error_dbus))
+      goto error_cleanup;
   }
   dbus_message_unref(message);
   dbus_message_unref(response);
   return true;
-cleanup:
+error_cleanup:
   if (dbus_error_is_set(&error_dbus))
     dbus_error_free(&error_dbus);
-  if (connection)
-    dbus_connection_unref(connection);
+repeat_inhibit_cleanup:
   if (message)
     dbus_message_unref(message);
   if (response)
@@ -110,7 +111,7 @@ bool ChangeScreenSaverStateDBus(const bool inhibit_requested, const char* progra
 static bool SetScreensaverInhibit(bool inhibit)
 {
 #ifdef USE_DBUS
-  return ChangeScreenSaverStateDBus(inhibit, "DuckStation", "DuckStation VM is running.");
+  return SetScreensaverInhibitorDBus(inhibit, "DuckStation", "DuckStation VM is running.");
 #else
 
   std::optional<WindowInfo> wi(Host::GetTopLevelWindowInfo());