diff --git a/include/SDL3/SDL_video.h b/include/SDL3/SDL_video.h
index b35d80113f18f..48cc46d7e0d3b 100644
--- a/include/SDL3/SDL_video.h
+++ b/include/SDL3/SDL_video.h
@@ -2703,6 +2703,18 @@ extern SDL_DECLSPEC bool SDLCALL SDL_SetWindowOpacity(SDL_Window *window, float
  */
 extern SDL_DECLSPEC float SDLCALL SDL_GetWindowOpacity(SDL_Window *window);
 
+/**
+ * Enable or disable mouse passthrough for a window.
+ *
+ * \param window the window to set mouse passthrough for.
+ * \param passthrough true to make the window transparent to mouse input, false to capture mouse input.
+ *
+ * \threadsafety This function should only be called on the main thread.
+ *
+ * \since This function is available since SDL 3.6.0.
+ */
+extern SDL_DECLSPEC void SDLCALL SDL_SetWindowMousePassthrough(SDL_Window *window, bool passthrough);
+
 /**
  * Set the window as a child of a parent window.
  *
diff --git a/src/dynapi/SDL_dynapi.sym b/src/dynapi/SDL_dynapi.sym
index de64a3efad92a..7b73836973e42 100644
--- a/src/dynapi/SDL_dynapi.sym
+++ b/src/dynapi/SDL_dynapi.sym
@@ -1270,6 +1270,7 @@ SDL3_0.0.0 {
     SDL_RotateSurface;
     SDL_LoadSurface_IO;
     SDL_LoadSurface;
+    SDL_SetWindowMousePassthrough;
     # extra symbols go here (don't modify this line)
   local: *;
 };
diff --git a/src/dynapi/SDL_dynapi_overrides.h b/src/dynapi/SDL_dynapi_overrides.h
index cc53044efb606..c708071706d9b 100644
--- a/src/dynapi/SDL_dynapi_overrides.h
+++ b/src/dynapi/SDL_dynapi_overrides.h
@@ -1296,3 +1296,4 @@
 #define SDL_RotateSurface SDL_RotateSurface_REAL
 #define SDL_LoadSurface_IO SDL_LoadSurface_IO_REAL
 #define SDL_LoadSurface SDL_LoadSurface_REAL
+#define SDL_SetWindowMousePassthrough SDL_SetWindowMousePassthrough_REAL
diff --git a/src/dynapi/SDL_dynapi_procs.h b/src/dynapi/SDL_dynapi_procs.h
index 9e3c9cdbef2bd..86e12f93832ea 100644
--- a/src/dynapi/SDL_dynapi_procs.h
+++ b/src/dynapi/SDL_dynapi_procs.h
@@ -1304,3 +1304,4 @@ SDL_DYNAPI_PROC(SDL_Cursor*,SDL_CreateAnimatedCursor,(SDL_CursorFrameInfo *a,int
 SDL_DYNAPI_PROC(SDL_Surface*,SDL_RotateSurface,(SDL_Surface *a,float b),(a,b),return)
 SDL_DYNAPI_PROC(SDL_Surface*,SDL_LoadSurface_IO,(SDL_IOStream *a,bool b),(a,b),return)
 SDL_DYNAPI_PROC(SDL_Surface*,SDL_LoadSurface,(const char *a),(a),return)
+SDL_DYNAPI_PROC(void,SDL_SetWindowMousePassthrough,(SDL_Window *a,bool b),(a,b),)
diff --git a/src/video/SDL_sysvideo.h b/src/video/SDL_sysvideo.h
index 27819d4e7c038..c2cfebc559369 100644
--- a/src/video/SDL_sysvideo.h
+++ b/src/video/SDL_sysvideo.h
@@ -284,6 +284,7 @@ struct SDL_VideoDevice
     float (*GetWindowContentScale)(SDL_VideoDevice *_this, SDL_Window *window);
     void (*GetWindowSizeInPixels)(SDL_VideoDevice *_this, SDL_Window *window, int *w, int *h);
     bool (*SetWindowOpacity)(SDL_VideoDevice *_this, SDL_Window *window, float opacity);
+    void (*SetWindowMousePassthrough)(SDL_VideoDevice *_this, SDL_Window *window, bool passthrough);
     bool (*SetWindowParent)(SDL_VideoDevice *_this, SDL_Window *window, SDL_Window *parent);
     bool (*SetWindowModal)(SDL_VideoDevice *_this, SDL_Window *window, bool modal);
     void (*ShowWindow)(SDL_VideoDevice *_this, SDL_Window *window);
diff --git a/src/video/SDL_video.c b/src/video/SDL_video.c
index 4f9bb6a437c86..f2a54442d8c2e 100644
--- a/src/video/SDL_video.c
+++ b/src/video/SDL_video.c
@@ -3793,6 +3793,16 @@ float SDL_GetWindowOpacity(SDL_Window *window)
     return window->opacity;
 }
 
+void SDL_SetWindowMousePassthrough(SDL_Window *window, bool passthrough)
+{
+    if (!_this->SetWindowMousePassthrough) {
+        SDL_Unsupported();
+        return;
+    }
+
+    _this->SetWindowMousePassthrough(_this, window, passthrough);
+}
+
 bool SDL_SetWindowParent(SDL_Window *window, SDL_Window *parent)
 {
     CHECK_WINDOW_MAGIC(window, false);
diff --git a/src/video/cocoa/SDL_cocoavideo.m b/src/video/cocoa/SDL_cocoavideo.m
index d77080779d848..55e5b39ddfcab 100644
--- a/src/video/cocoa/SDL_cocoavideo.m
+++ b/src/video/cocoa/SDL_cocoavideo.m
@@ -101,6 +101,7 @@ static void Cocoa_DeleteDevice(SDL_VideoDevice *device)
         device->SetWindowMaximumSize = Cocoa_SetWindowMaximumSize;
         device->SetWindowAspectRatio = Cocoa_SetWindowAspectRatio;
         device->SetWindowOpacity = Cocoa_SetWindowOpacity;
+        device->SetWindowMousePassthrough = Cocoa_SetWindowMousePassthrough;
         device->GetWindowSizeInPixels = Cocoa_GetWindowSizeInPixels;
         device->ShowWindow = Cocoa_ShowWindow;
         device->HideWindow = Cocoa_HideWindow;
diff --git a/src/video/cocoa/SDL_cocoawindow.h b/src/video/cocoa/SDL_cocoawindow.h
index f5ca4ab894960..1361713ebc27f 100644
--- a/src/video/cocoa/SDL_cocoawindow.h
+++ b/src/video/cocoa/SDL_cocoawindow.h
@@ -173,6 +173,7 @@ extern void Cocoa_SetWindowMaximumSize(SDL_VideoDevice *_this, SDL_Window *windo
 extern void Cocoa_SetWindowAspectRatio(SDL_VideoDevice *_this, SDL_Window *window);
 extern void Cocoa_GetWindowSizeInPixels(SDL_VideoDevice *_this, SDL_Window *window, int *w, int *h);
 extern bool Cocoa_SetWindowOpacity(SDL_VideoDevice *_this, SDL_Window *window, float opacity);
+extern void Cocoa_SetWindowMousePassthrough(SDL_VideoDevice *_this, SDL_Window *window, bool passthrough);
 extern void Cocoa_ShowWindow(SDL_VideoDevice *_this, SDL_Window *window);
 extern void Cocoa_HideWindow(SDL_VideoDevice *_this, SDL_Window *window);
 extern void Cocoa_RaiseWindow(SDL_VideoDevice *_this, SDL_Window *window);
diff --git a/src/video/cocoa/SDL_cocoawindow.m b/src/video/cocoa/SDL_cocoawindow.m
index d377bdbfc09e4..41a27fd463414 100644
--- a/src/video/cocoa/SDL_cocoawindow.m
+++ b/src/video/cocoa/SDL_cocoawindow.m
@@ -3416,6 +3416,13 @@ bool Cocoa_SetWindowOpacity(SDL_VideoDevice *_this, SDL_Window *window, float op
     }
 }
 
+void Cocoa_SetWindowMousePassthrough(SDL_VideoDevice *_this, SDL_Window *window, bool passthrough) {
+    @autoreleasepool {
+        SDL_CocoaWindowData *data = (__bridge SDL_CocoaWindowData *)window->internal;
+        [data.nswindow setIgnoresMouseEvents:passthrough];
+    }
+}
+
 bool Cocoa_SyncWindow(SDL_VideoDevice *_this, SDL_Window *window)
 {
     bool result = false;
diff --git a/src/video/wayland/SDL_waylandvideo.c b/src/video/wayland/SDL_waylandvideo.c
index 9cd6de66876e4..b8a8712e214ae 100644
--- a/src/video/wayland/SDL_waylandvideo.c
+++ b/src/video/wayland/SDL_waylandvideo.c
@@ -656,6 +656,7 @@ static SDL_VideoDevice *Wayland_CreateDevice(bool require_preferred_protocols)
     device->SetWindowParent = Wayland_SetWindowParent;
     device->SetWindowModal = Wayland_SetWindowModal;
     device->SetWindowOpacity = Wayland_SetWindowOpacity;
+    device->SetWindowMousePassthrough = Wayland_SetWindowMousePassthrough;
     device->SetWindowTitle = Wayland_SetWindowTitle;
     device->SetWindowIcon = Wayland_SetWindowIcon;
     device->GetWindowSizeInPixels = Wayland_GetWindowSizeInPixels;
diff --git a/src/video/wayland/SDL_waylandwindow.c b/src/video/wayland/SDL_waylandwindow.c
index 5fddec7221fda..2d6addb1f10f2 100644
--- a/src/video/wayland/SDL_waylandwindow.c
+++ b/src/video/wayland/SDL_waylandwindow.c
@@ -2961,6 +2961,20 @@ bool Wayland_SetWindowOpacity(SDL_VideoDevice *_this, SDL_Window *window, float
     return SDL_SetError("wayland: set window opacity failed; compositor lacks support for the required wp_alpha_modifier_v1 protocol");
 }
 
+void Wayland_SetWindowMousePassthrough(SDL_VideoDevice *_this, SDL_Window *window, bool passthrough)
+{
+    SDL_VideoData *viddata = _this->internal;
+    SDL_WindowData *data = window->internal;
+
+    if (passthrough) {
+        struct wl_region *region = wl_compositor_create_region(viddata->compositor);
+        wl_surface_set_input_region(data->surface, region);
+        wl_region_destroy(region);
+    } else {
+        wl_surface_set_input_region(data->surface, NULL);
+    }
+}
+
 void Wayland_SetWindowTitle(SDL_VideoDevice *_this, SDL_Window *window)
 {
     SDL_WindowData *wind = window->internal;
diff --git a/src/video/wayland/SDL_waylandwindow.h b/src/video/wayland/SDL_waylandwindow.h
index eeec232b7a9cc..3449bf4976fb5 100644
--- a/src/video/wayland/SDL_waylandwindow.h
+++ b/src/video/wayland/SDL_waylandwindow.h
@@ -243,6 +243,7 @@ extern SDL_DisplayID Wayland_GetDisplayForWindow(SDL_VideoDevice *_this, SDL_Win
 extern bool Wayland_SetWindowParent(SDL_VideoDevice *_this, SDL_Window *window, SDL_Window *parent_window);
 extern bool Wayland_SetWindowModal(SDL_VideoDevice *_this, SDL_Window *window, bool modal);
 extern bool Wayland_SetWindowOpacity(SDL_VideoDevice *_this, SDL_Window *window, float opacity);
+extern void Wayland_SetWindowMousePassthrough(SDL_VideoDevice *_this, SDL_Window *window, bool passthrough);
 extern void Wayland_SetWindowTitle(SDL_VideoDevice *_this, SDL_Window *window);
 extern void Wayland_ShowWindowSystemMenu(SDL_Window *window, int x, int y);
 extern void Wayland_DestroyWindow(SDL_VideoDevice *_this, SDL_Window *window);
diff --git a/src/video/windows/SDL_windowsvideo.c b/src/video/windows/SDL_windowsvideo.c
index 3db7614b46391..8484fe894e124 100644
--- a/src/video/windows/SDL_windowsvideo.c
+++ b/src/video/windows/SDL_windowsvideo.c
@@ -336,6 +336,7 @@ static SDL_VideoDevice *WIN_CreateDevice(void)
     device->GetWindowBordersSize = WIN_GetWindowBordersSize;
     device->GetWindowSizeInPixels = WIN_GetWindowSizeInPixels;
     device->SetWindowOpacity = WIN_SetWindowOpacity;
+    device->SetWindowMousePassthrough = WIN_SetWindowMousePassthrough;
     device->ShowWindow = WIN_ShowWindow;
     device->HideWindow = WIN_HideWindow;
     device->RaiseWindow = WIN_RaiseWindow;
diff --git a/src/video/windows/SDL_windowswindow.c b/src/video/windows/SDL_windowswindow.c
index b3cedbbf1c5ea..61fd7d31046ba 100644
--- a/src/video/windows/SDL_windowswindow.c
+++ b/src/video/windows/SDL_windowswindow.c
@@ -1675,6 +1675,35 @@ bool WIN_SetWindowOpacity(SDL_VideoDevice *_this, SDL_Window *window, float opac
 #endif // !defined(SDL_PLATFORM_XBOXONE) && !defined(SDL_PLATFORM_XBOXSERIES)
 }
 
+void WIN_SetWindowMousePassthrough(SDL_VideoDevice *_this, SDL_Window *window, bool passthrough)
+{
+#if defined(SDL_PLATFORM_XBOXONE) || defined(SDL_PLATFORM_XBOXSERIES)
+#else
+    SDL_WindowData *data = window->internal;
+    HWND hwnd = data->hwnd;
+    LONG style = GetWindowLong(hwnd, GWL_EXSTYLE);
+
+    if (passthrough) {
+        COLORREF key = 0;
+        BYTE alpha = 0;
+        DWORD flags = 0;
+        if (style & WS_EX_LAYERED) {
+            GetLayeredWindowAttributes(hwnd, &key, &alpha, &flags);
+        }
+        style |= (WS_EX_TRANSPARENT | WS_EX_LAYERED);
+        SetWindowLong(hwnd, GWL_EXSTYLE, style);
+        SetLayeredWindowAttributes(hwnd, key, alpha, flags);
+    } else {
+        style &= ~WS_EX_TRANSPARENT;
+
+        if ((style & (WS_EX_LAYERED | LWA_ALPHA)) == WS_EX_LAYERED) {
+            style &= ~WS_EX_LAYERED;
+        }
+        SetWindowLong(hwnd, GWL_EXSTYLE, style);
+    }
+#endif // !defined(SDL_PLATFORM_XBOXONE) && !defined(SDL_PLATFORM_XBOXSERIES)
+}
+
 #if !defined(SDL_PLATFORM_XBOXONE) && !defined(SDL_PLATFORM_XBOXSERIES)
 
 static const char *SDLGetClipboardFormatName(UINT cf, char *text, int len)
diff --git a/src/video/windows/SDL_windowswindow.h b/src/video/windows/SDL_windowswindow.h
index d461660d017d1..88f1537c26a05 100644
--- a/src/video/windows/SDL_windowswindow.h
+++ b/src/video/windows/SDL_windowswindow.h
@@ -115,6 +115,7 @@ extern void WIN_SetWindowSize(SDL_VideoDevice *_this, SDL_Window *window);
 extern bool WIN_GetWindowBordersSize(SDL_VideoDevice *_this, SDL_Window *window, int *top, int *left, int *bottom, int *right);
 extern void WIN_GetWindowSizeInPixels(SDL_VideoDevice *_this, SDL_Window *window, int *width, int *height);
 extern bool WIN_SetWindowOpacity(SDL_VideoDevice *_this, SDL_Window *window, float opacity);
+extern void WIN_SetWindowMousePassthrough(SDL_VideoDevice *_this, SDL_Window *window, bool passthrough);
 extern void WIN_ShowWindow(SDL_VideoDevice *_this, SDL_Window *window);
 extern void WIN_HideWindow(SDL_VideoDevice *_this, SDL_Window *window);
 extern void WIN_RaiseWindow(SDL_VideoDevice *_this, SDL_Window *window);
diff --git a/src/video/x11/SDL_x11video.c b/src/video/x11/SDL_x11video.c
index 55002abe45c54..d12750db837d3 100644
--- a/src/video/x11/SDL_x11video.c
+++ b/src/video/x11/SDL_x11video.c
@@ -161,6 +161,7 @@ static SDL_VideoDevice *X11_CreateDevice(void)
     device->SetWindowAspectRatio = X11_SetWindowAspectRatio;
     device->GetWindowBordersSize = X11_GetWindowBordersSize;
     device->SetWindowOpacity = X11_SetWindowOpacity;
+    device->SetWindowMousePassthrough = X11_SetWindowMousePassthrough;
     device->SetWindowParent = X11_SetWindowParent;
     device->SetWindowModal = X11_SetWindowModal;
     device->ShowWindow = X11_ShowWindow;
diff --git a/src/video/x11/SDL_x11window.c b/src/video/x11/SDL_x11window.c
index b44690878825e..57b616d23c41f 100644
--- a/src/video/x11/SDL_x11window.c
+++ b/src/video/x11/SDL_x11window.c
@@ -1395,6 +1395,20 @@ bool X11_SetWindowOpacity(SDL_VideoDevice *_this, SDL_Window *window, float opac
     return true;
 }
 
+void X11_SetWindowMousePassthrough(SDL_VideoDevice *_this, SDL_Window *window, bool passthrough)
+{
+    SDL_WindowData *data = window->internal;
+    Display *display = data->videodata->display;
+
+    if (passthrough) {
+        Region region = X11_XCreateRegion();
+        X11_XShapeCombineRegion(display, data->xwindow, ShapeInput, 0, 0, region, ShapeSet);
+        X11_XDestroyRegion(region);
+    } else {
+        X11_XShapeCombineMask(display, data->xwindow, ShapeInput, 0, 0, None, ShapeSet);
+    }
+}
+
 bool X11_SetWindowParent(SDL_VideoDevice *_this, SDL_Window *window, SDL_Window *parent)
 {
     SDL_WindowData *data = window->internal;
diff --git a/src/video/x11/SDL_x11window.h b/src/video/x11/SDL_x11window.h
index a7fad8982b14e..00210a6751b4d 100644
--- a/src/video/x11/SDL_x11window.h
+++ b/src/video/x11/SDL_x11window.h
@@ -141,6 +141,7 @@ extern void X11_SetWindowMaximumSize(SDL_VideoDevice *_this, SDL_Window *window)
 extern void X11_SetWindowAspectRatio(SDL_VideoDevice *_this, SDL_Window *window);
 extern bool X11_GetWindowBordersSize(SDL_VideoDevice *_this, SDL_Window *window, int *top, int *left, int *bottom, int *right);
 extern bool X11_SetWindowOpacity(SDL_VideoDevice *_this, SDL_Window *window, float opacity);
+extern void X11_SetWindowMousePassthrough(SDL_VideoDevice *_this, SDL_Window *window, bool passthrough);
 extern bool X11_SetWindowParent(SDL_VideoDevice *_this, SDL_Window *window, SDL_Window *parent);
 extern bool X11_SetWindowModal(SDL_VideoDevice *_this, SDL_Window *window, bool modal);
 extern void X11_SetWindowSize(SDL_VideoDevice *_this, SDL_Window *window);