diff --git a/src/video/SDL_video.c b/src/video/SDL_video.c
index d1e24eaaa0..2a5b419a24 100644
--- a/src/video/SDL_video.c
+++ b/src/video/SDL_video.c
@@ -1562,6 +1562,10 @@ void SDL_RelativeToGlobalForWindow(SDL_Window *window, int rel_x, int rel_y, int
         for (w = window->parent; w; w = w->parent) {
             rel_x += w->x;
             rel_y += w->y;
+
+            if (!SDL_WINDOW_IS_POPUP(w)) {
+                break;
+            }
         }
     }
 
@@ -1582,6 +1586,10 @@ void SDL_GlobalToRelativeForWindow(SDL_Window *window, int abs_x, int abs_y, int
         for (w = window->parent; w; w = w->parent) {
             abs_x -= w->x;
             abs_y -= w->y;
+
+            if (!SDL_WINDOW_IS_POPUP(w)) {
+                break;
+            }
         }
     }
 
diff --git a/src/video/cocoa/SDL_cocoawindow.m b/src/video/cocoa/SDL_cocoawindow.m
index bafeda0ddd..4f51a514fe 100644
--- a/src/video/cocoa/SDL_cocoawindow.m
+++ b/src/video/cocoa/SDL_cocoawindow.m
@@ -622,26 +622,29 @@ static void Cocoa_UpdateClipCursor(SDL_Window *window)
     }
 }
 
-static SDL_Window *GetTopmostWindow(SDL_Window *window)
+static SDL_Window *GetParentToplevelWindow(SDL_Window *window)
 {
-    SDL_Window *topmost = window;
+    SDL_Window *toplevel = window;
 
     // Find the topmost parent
-    while (topmost->parent != NULL) {
-        topmost = topmost->parent;
+    while (SDL_WINDOW_IS_POPUP(toplevel)) {
+        toplevel = toplevel->parent;
     }
 
-    return topmost;
+    return toplevel;
 }
 
 static void Cocoa_SetKeyboardFocus(SDL_Window *window)
 {
-    SDL_Window *topmost = GetTopmostWindow(window);
-    SDL_CocoaWindowData *topmost_data;
+    SDL_Window *toplevel = GetParentToplevelWindow(window);
+    SDL_CocoaWindowData *toplevel_data;
 
-    topmost_data = (__bridge SDL_CocoaWindowData *)topmost->internal;
-    topmost_data.keyboard_focus = window;
-    SDL_SetKeyboardFocus(window);
+    toplevel_data = (__bridge SDL_CocoaWindowData *)toplevel->internal;
+    toplevel_data.keyboard_focus = window;
+
+    if (!window->is_hiding && !window->is_destroying) {
+    	SDL_SetKeyboardFocus(window);
+    }
 }
 
 static void Cocoa_SendExposedEventIfVisible(SDL_Window *window)
@@ -2555,8 +2558,8 @@ void Cocoa_HideWindow(SDL_VideoDevice *_this, SDL_Window *window)
             if (window == SDL_GetKeyboardFocus()) {
                 SDL_Window *new_focus = window->parent;
 
-                // Find the highest level window that isn't being hidden or destroyed.
-                while (new_focus->parent != NULL && (new_focus->is_hiding || new_focus->is_destroying)) {
+                // Find the highest level window, up to the next toplevel, that isn't being hidden or destroyed.
+                while (SDL_WINDOW_IS_POPUP(new_focus) && (new_focus->is_hiding || new_focus->is_destroying)) {
                     new_focus = new_focus->parent;
                 }
 
@@ -2988,7 +2991,7 @@ void Cocoa_DestroyWindow(SDL_VideoDevice *_this, SDL_Window *window)
             NSArray *contexts;
 
 #endif // SDL_VIDEO_OPENGL
-            SDL_Window *topmost = GetTopmostWindow(window);
+            SDL_Window *topmost = GetParentToplevelWindow(window);
             SDL_CocoaWindowData *topmost_data = (__bridge SDL_CocoaWindowData *)topmost->internal;
 
             /* Reset the input focus of the root window if this window is still set as keyboard focus.
@@ -2998,7 +3001,7 @@ void Cocoa_DestroyWindow(SDL_VideoDevice *_this, SDL_Window *window)
              */
             if (topmost_data.keyboard_focus == window) {
                 SDL_Window *new_focus = window;
-                while (new_focus->parent && (new_focus->is_hiding || new_focus->is_destroying)) {
+                while (SDL_WINDOW_IS_POPUP(new_focus) && (new_focus->is_hiding || new_focus->is_destroying)) {
                     new_focus = new_focus->parent;
                 }
 
diff --git a/src/video/wayland/SDL_waylandwindow.c b/src/video/wayland/SDL_waylandwindow.c
index 4b2616de7f..75e80af4ee 100644
--- a/src/video/wayland/SDL_waylandwindow.c
+++ b/src/video/wayland/SDL_waylandwindow.c
@@ -1631,16 +1631,18 @@ static const struct frog_color_managed_surface_listener frog_surface_listener =
 
 static void SetKeyboardFocus(SDL_Window *window)
 {
-    SDL_Window *topmost = window;
+    SDL_Window *toplevel = window;
 
-    // Find the topmost parent
-    while (topmost->parent) {
-        topmost = topmost->parent;
+    // Find the toplevel parent
+    while (SDL_WINDOW_IS_POPUP(toplevel)) {
+        toplevel = toplevel->parent;
     }
 
-    topmost->internal->keyboard_focus = window;
+    toplevel->internal->keyboard_focus = window;
 
-    SDL_SetKeyboardFocus(window);
+    if (!window->is_hiding && !window->is_destroying) {
+        SDL_SetKeyboardFocus(window);
+    }
 }
 
 bool Wayland_SetWindowHitTest(SDL_Window *window, bool enabled)
@@ -2043,8 +2045,8 @@ static void Wayland_ReleasePopup(SDL_VideoDevice *_this, SDL_Window *popup)
         if (popup == SDL_GetKeyboardFocus()) {
             SDL_Window *new_focus = popup->parent;
 
-            // Find the highest level window that isn't being hidden or destroyed.
-            while (new_focus->parent && (new_focus->is_hiding || new_focus->is_destroying)) {
+            // Find the highest level window, up to the toplevel parent, that isn't being hidden or destroyed.
+            while (SDL_WINDOW_IS_POPUP(new_focus) && new_focus->parent && (new_focus->is_hiding || new_focus->is_destroying)) {
                 new_focus = new_focus->parent;
             }
 
diff --git a/src/video/windows/SDL_windowsevents.c b/src/video/windows/SDL_windowsevents.c
index de3d3a6a2c..51fbbe9f9c 100644
--- a/src/video/windows/SDL_windowsevents.c
+++ b/src/video/windows/SDL_windowsevents.c
@@ -1533,8 +1533,8 @@ LRESULT CALLBACK WIN_WindowProc(HWND hwnd, UINT msg, WPARAM wParam, LPARAM lPara
 
         // Update the position of any child windows
         for (win = data->window->first_child; win; win = win->next_sibling) {
-            // Don't update hidden child windows, their relative position doesn't change
-            if (!(win->flags & SDL_WINDOW_HIDDEN)) {
+            // Don't update hidden child popup windows, their relative position doesn't change
+            if (SDL_WINDOW_IS_POPUP(win) && !(win->flags & SDL_WINDOW_HIDDEN)) {
                 WIN_SetWindowPositionInternal(win, SWP_NOCOPYBITS | SWP_NOACTIVATE, SDL_WINDOWRECT_CURRENT);
             }
         }
diff --git a/src/video/windows/SDL_windowswindow.c b/src/video/windows/SDL_windowswindow.c
index 0286aaf33c..d4456cab3b 100644
--- a/src/video/windows/SDL_windowswindow.c
+++ b/src/video/windows/SDL_windowswindow.c
@@ -687,7 +687,7 @@ static void WIN_ConstrainPopup(SDL_Window *window, bool output_to_pending)
         int offset_x = 0, offset_y = 0;
 
         // Calculate the total offset from the parents
-        for (w = window->parent; w->parent; w = w->parent) {
+        for (w = window->parent; SDL_WINDOW_IS_POPUP(w); w = w->parent) {
             offset_x += w->x;
             offset_y += w->y;
         }
@@ -725,15 +725,18 @@ static void WIN_ConstrainPopup(SDL_Window *window, bool output_to_pending)
 
 static void WIN_SetKeyboardFocus(SDL_Window *window)
 {
-    SDL_Window *topmost = window;
+    SDL_Window *toplevel = window;
 
     // Find the topmost parent
-    while (topmost->parent) {
-        topmost = topmost->parent;
+    while (SDL_WINDOW_IS_POPUP(toplevel)) {
+        toplevel = toplevel->parent;
     }
 
-    topmost->internal->keyboard_focus = window;
-    SDL_SetKeyboardFocus(window);
+    toplevel->internal->keyboard_focus = window;
+
+    if (!window->is_hiding && !window->is_destroying) {
+    	SDL_SetKeyboardFocus(window);
+    }
 }
 
 bool WIN_CreateWindow(SDL_VideoDevice *_this, SDL_Window *window, SDL_PropertiesID create_props)
@@ -1118,8 +1121,8 @@ void WIN_HideWindow(SDL_VideoDevice *_this, SDL_Window *window)
         if (window == SDL_GetKeyboardFocus()) {
             SDL_Window *new_focus = window->parent;
 
-            // Find the highest level window that isn't being hidden or destroyed.
-            while (new_focus->parent && (new_focus->is_hiding || new_focus->is_destroying)) {
+            // Find the highest level window, up to the toplevel parent, that isn't being hidden or destroyed.
+            while (SDL_WINDOW_IS_POPUP(new_focus) && (new_focus->is_hiding || new_focus->is_destroying)) {
                 new_focus = new_focus->parent;
             }
 
diff --git a/src/video/x11/SDL_x11events.c b/src/video/x11/SDL_x11events.c
index ad46ffbd0d..9baf943aa6 100644
--- a/src/video/x11/SDL_x11events.c
+++ b/src/video/x11/SDL_x11events.c
@@ -1382,8 +1382,8 @@ static void X11_DispatchEvent(SDL_VideoDevice *_this, XEvent *xevent)
                 }
 #endif
                 for (w = data->window->first_child; w; w = w->next_sibling) {
-                    // Don't update hidden child windows, their relative position doesn't change
-                    if (!(w->flags & SDL_WINDOW_HIDDEN)) {
+                    // Don't update hidden child popup windows, their relative position doesn't change
+                    if (SDL_WINDOW_IS_POPUP(w) && !(w->flags & SDL_WINDOW_HIDDEN)) {
                         X11_UpdateWindowPosition(w, true);
                     }
                 }
diff --git a/src/video/x11/SDL_x11window.c b/src/video/x11/SDL_x11window.c
index 816f51d537..791d515e19 100644
--- a/src/video/x11/SDL_x11window.c
+++ b/src/video/x11/SDL_x11window.c
@@ -208,7 +208,7 @@ static void X11_ConstrainPopup(SDL_Window *window, bool output_to_pending)
         int offset_x = 0, offset_y = 0;
 
         // Calculate the total offset from the parents
-        for (w = window->parent; w->parent; w = w->parent) {
+        for (w = window->parent; SDL_WINDOW_IS_POPUP(w); w = w->parent) {
             offset_x += w->x;
             offset_y += w->y;
         }
@@ -242,15 +242,18 @@ static void X11_ConstrainPopup(SDL_Window *window, bool output_to_pending)
 
 static void X11_SetKeyboardFocus(SDL_Window *window)
 {
-    SDL_Window *topmost = window;
+    SDL_Window *toplevel = window;
 
-    // Find the topmost parent
-    while (topmost->parent) {
-        topmost = topmost->parent;
+    // Find the toplevel parent
+    while (SDL_WINDOW_IS_POPUP(toplevel)) {
+        toplevel = toplevel->parent;
     }
 
-    topmost->internal->keyboard_focus = window;
-    SDL_SetKeyboardFocus(window);
+    toplevel->internal->keyboard_focus = window;
+
+    if (!window->is_hiding && !window->is_destroying) {
+        SDL_SetKeyboardFocus(window);
+    }
 }
 
 Uint32 X11_GetNetWMState(SDL_VideoDevice *_this, SDL_Window *window, Window xwindow)
@@ -1533,7 +1536,7 @@ void X11_HideWindow(SDL_VideoDevice *_this, SDL_Window *window)
             SDL_Window *new_focus = window->parent;
 
             // Find the highest level window that isn't being hidden or destroyed.
-            while (new_focus->parent && (new_focus->is_hiding || new_focus->is_destroying)) {
+            while (SDL_WINDOW_IS_POPUP(new_focus) && (new_focus->is_hiding || new_focus->is_destroying)) {
                 new_focus = new_focus->parent;
             }