diff --git a/Source/Core/Core/Core.cpp b/Source/Core/Core/Core.cpp
index fff3e6bfff..b5a4b13ce0 100644
--- a/Source/Core/Core/Core.cpp
+++ b/Source/Core/Core/Core.cpp
@@ -456,6 +456,10 @@ static void EmuThread(std::unique_ptr<BootParameters> boot, WindowSystemInfo wsi
     return;
   }
 
+  // The frontend will likely have initialized the controller interface, as it needs
+  // it to provide the configuration dialogs. In this case, instead of re-initializing
+  // entirely, we switch the window used for inputs to the render window. This way, the
+  // cursor position is relative to the render window, instead of the main window.
   bool init_controllers = false;
   if (!g_controller_interface.IsInit())
   {
@@ -467,6 +471,7 @@ static void EmuThread(std::unique_ptr<BootParameters> boot, WindowSystemInfo wsi
   else
   {
     // Update references in case controllers were refreshed
+    g_controller_interface.ChangeWindow(wsi.render_surface);
     Pad::LoadConfig();
     Keyboard::LoadConfig();
   }
diff --git a/Source/Core/DolphinQt/MainWindow.cpp b/Source/Core/DolphinQt/MainWindow.cpp
index f02542da95..e2b9e15791 100644
--- a/Source/Core/DolphinQt/MainWindow.cpp
+++ b/Source/Core/DolphinQt/MainWindow.cpp
@@ -940,6 +940,11 @@ void MainWindow::HideRenderWidget(bool reinit)
       if (m_render_widget->isFullScreen())
         SetFullScreenResolution(focus);
     });
+
+    // The controller interface will still be registered to the old render widget, if the core
+    // has booted. Therefore, we should re-bind it to the main window for now. When the core
+    // is next started, it will be swapped back to the new render widget.
+    g_controller_interface.ChangeWindow(GetWindowSystemInfo(windowHandle()).render_surface);
   }
 }
 
diff --git a/Source/Core/InputCommon/ControllerInterface/ControllerInterface.cpp b/Source/Core/InputCommon/ControllerInterface/ControllerInterface.cpp
index 7be22d4a8d..9f6e7c5179 100644
--- a/Source/Core/InputCommon/ControllerInterface/ControllerInterface.cpp
+++ b/Source/Core/InputCommon/ControllerInterface/ControllerInterface.cpp
@@ -80,6 +80,15 @@ void ControllerInterface::Initialize(const WindowSystemInfo& wsi)
   RefreshDevices();
 }
 
+void ControllerInterface::ChangeWindow(void* hwnd)
+{
+  if (!m_is_init)
+    return;
+
+  m_wsi.render_surface = hwnd;
+  RefreshDevices();
+}
+
 void ControllerInterface::RefreshDevices()
 {
   if (!m_is_init)
diff --git a/Source/Core/InputCommon/ControllerInterface/ControllerInterface.h b/Source/Core/InputCommon/ControllerInterface/ControllerInterface.h
index 2e078e8934..d5567222a4 100644
--- a/Source/Core/InputCommon/ControllerInterface/ControllerInterface.h
+++ b/Source/Core/InputCommon/ControllerInterface/ControllerInterface.h
@@ -42,6 +42,7 @@ class ControllerInterface : public ciface::Core::DeviceContainer
 public:
   ControllerInterface() : m_is_init(false) {}
   void Initialize(const WindowSystemInfo& wsi);
+  void ChangeWindow(void* hwnd);
   void RefreshDevices();
   void Shutdown();
   void AddDevice(std::shared_ptr<ciface::Core::Device> device);