diff --git a/Source/Android/jni/MainAndroid.cpp b/Source/Android/jni/MainAndroid.cpp
index 9fcf1b33a3..cb1a252d3c 100644
--- a/Source/Android/jni/MainAndroid.cpp
+++ b/Source/Android/jni/MainAndroid.cpp
@@ -173,6 +173,11 @@ bool Host_RendererIsFullscreen()
   return false;
 }
 
+bool Host_TASInputHasFocus()
+{
+  return false;
+}
+
 void Host_YieldToUI()
 {
 }
diff --git a/Source/Core/Core/Core.cpp b/Source/Core/Core/Core.cpp
index 5c60b3b02f..bae5b15258 100644
--- a/Source/Core/Core/Core.cpp
+++ b/Source/Core/Core/Core.cpp
@@ -1073,7 +1073,8 @@ void UpdateInputGate(bool require_focus, bool require_full_focus)
 {
   // If the user accepts background input, controls should pass even if an on screen interface is on
   const bool focus_passes =
-      !require_focus || (Host_RendererHasFocus() && !Host_UIBlocksControllerState());
+      !require_focus ||
+      ((Host_RendererHasFocus() || Host_TASInputHasFocus()) && !Host_UIBlocksControllerState());
   // Ignore full focus if we don't require basic focus
   const bool full_focus_passes =
       !require_focus || !require_full_focus || (focus_passes && Host_RendererHasFullFocus());
diff --git a/Source/Core/Core/Host.h b/Source/Core/Core/Host.h
index 8d22e9d59a..66a5e2d78e 100644
--- a/Source/Core/Core/Host.h
+++ b/Source/Core/Core/Host.h
@@ -53,6 +53,7 @@ bool Host_UIBlocksControllerState();
 bool Host_RendererHasFocus();
 bool Host_RendererHasFullFocus();
 bool Host_RendererIsFullscreen();
+bool Host_TASInputHasFocus();
 
 void Host_Message(HostMessageID id);
 void Host_PPCSymbolsChanged();
diff --git a/Source/Core/DolphinNoGUI/MainNoGUI.cpp b/Source/Core/DolphinNoGUI/MainNoGUI.cpp
index 6cbb2750d2..40145e6e4c 100644
--- a/Source/Core/DolphinNoGUI/MainNoGUI.cpp
+++ b/Source/Core/DolphinNoGUI/MainNoGUI.cpp
@@ -111,6 +111,11 @@ bool Host_RendererIsFullscreen()
   return s_platform->IsWindowFullscreen();
 }
 
+bool Host_TASInputHasFocus()
+{
+  return false;
+}
+
 void Host_YieldToUI()
 {
 }
diff --git a/Source/Core/DolphinQt/Host.cpp b/Source/Core/DolphinQt/Host.cpp
index fe339364ab..bb912a7ab2 100644
--- a/Source/Core/DolphinQt/Host.cpp
+++ b/Source/Core/DolphinQt/Host.cpp
@@ -162,6 +162,11 @@ bool Host::GetGBAFocus()
 #endif
 }
 
+bool Host::GetTASInputFocus() const
+{
+  return m_tas_input_focus;
+}
+
 bool Host::GetRenderFullscreen()
 {
   return m_render_fullscreen;
@@ -177,6 +182,11 @@ void Host::SetRenderFullscreen(bool fullscreen)
   }
 }
 
+void Host::SetTASInputFocus(const bool focus)
+{
+  m_tas_input_focus = focus;
+}
+
 void Host::ResizeSurface(int new_width, int new_height)
 {
   if (g_presenter)
@@ -228,6 +238,11 @@ bool Host_RendererIsFullscreen()
   return Host::GetInstance()->GetRenderFullscreen();
 }
 
+bool Host_TASInputHasFocus()
+{
+  return Host::GetInstance()->GetTASInputFocus();
+}
+
 void Host_YieldToUI()
 {
   qApp->processEvents(QEventLoop::ExcludeUserInputEvents);
diff --git a/Source/Core/DolphinQt/Host.h b/Source/Core/DolphinQt/Host.h
index 645c4bd54d..b7f21190da 100644
--- a/Source/Core/DolphinQt/Host.h
+++ b/Source/Core/DolphinQt/Host.h
@@ -25,12 +25,14 @@ public:
   bool GetRenderFullFocus();
   bool GetRenderFullscreen();
   bool GetGBAFocus();
+  bool GetTASInputFocus() const;
 
   void SetMainWindowHandle(void* handle);
   void SetRenderHandle(void* handle);
   void SetRenderFocus(bool focus);
   void SetRenderFullFocus(bool focus);
   void SetRenderFullscreen(bool fullscreen);
+  void SetTASInputFocus(bool focus);
   void ResizeSurface(int new_width, int new_height);
 
 signals:
@@ -49,4 +51,5 @@ private:
   std::atomic<bool> m_render_focus{false};
   std::atomic<bool> m_render_full_focus{false};
   std::atomic<bool> m_render_fullscreen{false};
+  std::atomic<bool> m_tas_input_focus{false};
 };
diff --git a/Source/Core/DolphinQt/TAS/TASInputWindow.cpp b/Source/Core/DolphinQt/TAS/TASInputWindow.cpp
index 604a564991..d3dc078375 100644
--- a/Source/Core/DolphinQt/TAS/TASInputWindow.cpp
+++ b/Source/Core/DolphinQt/TAS/TASInputWindow.cpp
@@ -6,7 +6,9 @@
 #include <cmath>
 #include <utility>
 
+#include <QApplication>
 #include <QCheckBox>
+#include <QEvent>
 #include <QGroupBox>
 #include <QHBoxLayout>
 #include <QLabel>
@@ -17,6 +19,7 @@
 
 #include "Common/CommonTypes.h"
 
+#include "DolphinQt/Host.h"
 #include "DolphinQt/QtUtils/AspectRatioWidget.h"
 #include "DolphinQt/QtUtils/QueueOnObject.h"
 #include "DolphinQt/Resources.h"
@@ -268,3 +271,16 @@ std::optional<ControlState> TASInputWindow::GetSpinBox(TASSpinBox* spin, int zer
 
   return (spin->GetValue() - zero) / scale;
 }
+
+void TASInputWindow::changeEvent(QEvent* const event)
+{
+  if (event->type() == QEvent::ActivationChange)
+  {
+    const bool active_window_is_tas_input =
+        qobject_cast<TASInputWindow*>(QApplication::activeWindow()) != nullptr;
+
+    // Switching between TAS Input windows will call SetTASInputFocus(true) twice, but that's fine.
+    Host::GetInstance()->SetTASInputFocus(active_window_is_tas_input);
+  }
+  QDialog::changeEvent(event);
+}
diff --git a/Source/Core/DolphinQt/TAS/TASInputWindow.h b/Source/Core/DolphinQt/TAS/TASInputWindow.h
index 34cc843633..924e53ac87 100644
--- a/Source/Core/DolphinQt/TAS/TASInputWindow.h
+++ b/Source/Core/DolphinQt/TAS/TASInputWindow.h
@@ -18,6 +18,7 @@
 class QBoxLayout;
 class QCheckBox;
 class QDialog;
+class QEvent;
 class QGroupBox;
 class QSpinBox;
 class QString;
@@ -68,6 +69,8 @@ protected:
                                     QKeySequence shortcut_key_sequence, Qt::Orientation orientation,
                                     QWidget* shortcut_widget);
 
+  void changeEvent(QEvent* event) override;
+
   QGroupBox* m_settings_box;
   QCheckBox* m_use_controller;
   QSpinBox* m_turbo_press_frames;
diff --git a/Source/Core/DolphinTool/ToolHeadlessPlatform.cpp b/Source/Core/DolphinTool/ToolHeadlessPlatform.cpp
index 8c1772406f..0b04cbfa19 100644
--- a/Source/Core/DolphinTool/ToolHeadlessPlatform.cpp
+++ b/Source/Core/DolphinTool/ToolHeadlessPlatform.cpp
@@ -84,6 +84,11 @@ bool Host_RendererIsFullscreen()
   return false;
 }
 
+bool Host_TASInputHasFocus()
+{
+  return false;
+}
+
 void Host_YieldToUI()
 {
 }
diff --git a/Source/Core/InputCommon/ControllerInterface/DInput/DInputKeyboardMouse.cpp b/Source/Core/InputCommon/ControllerInterface/DInput/DInputKeyboardMouse.cpp
index 3c6a82dcd8..8d7f7c7ada 100644
--- a/Source/Core/InputCommon/ControllerInterface/DInput/DInputKeyboardMouse.cpp
+++ b/Source/Core/InputCommon/ControllerInterface/DInput/DInputKeyboardMouse.cpp
@@ -179,7 +179,8 @@ void KeyboardMouse::UpdateCursorInput()
   const auto win_height = std::max(rect.bottom - rect.top, 1l);
 
   POINT point = {};
-  if (g_controller_interface.IsMouseCenteringRequested() && Host_RendererHasFocus())
+  if (g_controller_interface.IsMouseCenteringRequested() &&
+      (Host_RendererHasFocus() || Host_TASInputHasFocus()))
   {
     point.x = win_width / 2;
     point.y = win_height / 2;
@@ -189,6 +190,15 @@ void KeyboardMouse::UpdateCursorInput()
     SetCursorPos(screen_point.x, screen_point.y);
     g_controller_interface.SetMouseCenteringRequested(false);
   }
+  else if (Host_TASInputHasFocus())
+  {
+    // When a TAS Input window has focus and "Enable Controller Input" is checked most types of
+    // input should be read normally as if the render window had focus instead. The cursor is an
+    // exception, as otherwise using the mouse to set any control in the TAS Input window will also
+    // update the Wii IR value (or any other input controlled by the cursor).
+
+    return;
+  }
   else
   {
     GetCursorPos(&point);
diff --git a/Source/Core/InputCommon/ControllerInterface/Quartz/QuartzKeyboardAndMouse.mm b/Source/Core/InputCommon/ControllerInterface/Quartz/QuartzKeyboardAndMouse.mm
index 55f212900d..9a8ddfc6df 100644
--- a/Source/Core/InputCommon/ControllerInterface/Quartz/QuartzKeyboardAndMouse.mm
+++ b/Source/Core/InputCommon/ControllerInterface/Quartz/QuartzKeyboardAndMouse.mm
@@ -244,7 +244,8 @@ Core::DeviceRemoval KeyboardAndMouse::UpdateInput()
   const double window_width = std::max(bounds.size.width, 1.0);
   const double window_height = std::max(bounds.size.height, 1.0);
 
-  if (g_controller_interface.IsMouseCenteringRequested() && Host_RendererHasFocus())
+  if (g_controller_interface.IsMouseCenteringRequested() &&
+      (Host_RendererHasFocus() || Host_TASInputHasFocus()))
   {
     m_cursor.x = 0;
     m_cursor.y = 0;
@@ -258,8 +259,13 @@ Core::DeviceRemoval KeyboardAndMouse::UpdateInput()
 
     g_controller_interface.SetMouseCenteringRequested(false);
   }
-  else
+  else if (!Host_TASInputHasFocus())
   {
+    // When a TAS Input window has focus and "Enable Controller Input" is checked most types of
+    // input should be read normally as if the render window had focus instead. The cursor is an
+    // exception, as otherwise using the mouse to set any control in the TAS Input window will also
+    // update the Wii IR value (or any other input controlled by the cursor).
+
     NSPoint loc = [NSEvent mouseLocation];
 
     const auto window_scale = g_controller_interface.GetWindowInputScale();
diff --git a/Source/Core/InputCommon/ControllerInterface/Xlib/XInput2.cpp b/Source/Core/InputCommon/ControllerInterface/Xlib/XInput2.cpp
index e4b717e3af..057d774c5b 100644
--- a/Source/Core/InputCommon/ControllerInterface/Xlib/XInput2.cpp
+++ b/Source/Core/InputCommon/ControllerInterface/Xlib/XInput2.cpp
@@ -391,9 +391,16 @@ Core::DeviceRemoval KeyboardMouse::UpdateInput()
   m_state.axis.z += delta_z;
   m_state.axis.z /= SCROLL_AXIS_DECAY;
 
-  const bool should_center_mouse =
-      g_controller_interface.IsMouseCenteringRequested() && Host_RendererHasFocus();
-  if (update_mouse || should_center_mouse)
+  const bool should_center_mouse = g_controller_interface.IsMouseCenteringRequested() &&
+                                   (Host_RendererHasFocus() || Host_TASInputHasFocus());
+
+  // When a TAS Input window has focus and "Enable Controller Input" is checked most types of
+  // input should be read normally as if the render window had focus instead. The cursor is an
+  // exception, as otherwise using the mouse to set any control in the TAS Input window will also
+  // update the Wii IR value (or any other input controlled by the cursor).
+  const bool should_update_mouse = update_mouse && !Host_TASInputHasFocus();
+
+  if (should_update_mouse || should_center_mouse)
     UpdateCursor(should_center_mouse);
 
   if (update_keyboard)
diff --git a/Source/DSPTool/StubHost.cpp b/Source/DSPTool/StubHost.cpp
index d32346a457..e270acb23a 100644
--- a/Source/DSPTool/StubHost.cpp
+++ b/Source/DSPTool/StubHost.cpp
@@ -59,6 +59,10 @@ bool Host_RendererIsFullscreen()
 {
   return false;
 }
+bool Host_TASInputHasFocus()
+{
+  return false;
+}
 void Host_YieldToUI()
 {
 }
diff --git a/Source/UnitTests/StubHost.cpp b/Source/UnitTests/StubHost.cpp
index 47200bd40c..dc7dfe2277 100644
--- a/Source/UnitTests/StubHost.cpp
+++ b/Source/UnitTests/StubHost.cpp
@@ -63,6 +63,10 @@ bool Host_RendererIsFullscreen()
 {
   return false;
 }
+bool Host_TASInputHasFocus()
+{
+  return false;
+}
 void Host_YieldToUI()
 {
 }