diff --git a/src/citra_qt/bootmanager.cpp b/src/citra_qt/bootmanager.cpp
index d44ddb0968..6d08d6afc5 100644
--- a/src/citra_qt/bootmanager.cpp
+++ b/src/citra_qt/bootmanager.cpp
@@ -123,9 +123,6 @@ GRenderWindow::GRenderWindow(QWidget* parent) : QWidget(parent), emu_thread(this
     std::string window_title = Common::StringFromFormat("Citra | %s-%s", Common::g_scm_branch, Common::g_scm_desc);
     setWindowTitle(QString::fromStdString(window_title));
 
-    // Allow manually setting focus to the widget.
-    setFocusPolicy(Qt::ClickFocus);
-
     keyboard_id = KeyMap::NewDeviceId();
     ReloadSetKeymaps();
 
diff --git a/src/citra_qt/main.cpp b/src/citra_qt/main.cpp
index 9fc8705e66..37d69ac13c 100644
--- a/src/citra_qt/main.cpp
+++ b/src/citra_qt/main.cpp
@@ -170,7 +170,13 @@ void GMainWindow::BootGame(std::string filename)
     render_window->GetEmuThread().start();
 
     render_window->show();
-    render_window->setFocus();
+
+    // Allow manually setting focus to the render widget if not using popout mode.
+    if (!ui.action_Popout_Window_Mode->isChecked()) {
+        render_window->setFocusPolicy(Qt::ClickFocus);
+        render_window->setFocus();
+    }
+
     OnStartGame();
 }
 
@@ -231,12 +237,15 @@ void GMainWindow::ToggleWindowMode()
         render_window->setParent(nullptr);
         render_window->setVisible(true);
         render_window->RestoreGeometry();
+        render_window->setFocusPolicy(Qt::NoFocus);
     }
     else if (!enable && render_window->parent() == nullptr)
     {
         render_window->BackupGeometry();
         ui.horizontalLayout->addWidget(render_window);
         render_window->setVisible(true);
+        render_window->setFocusPolicy(Qt::ClickFocus);
+        render_window->setFocus();
     }
 }