diff --git a/lisp/doom-editor.el b/lisp/doom-editor.el
index f3ec6efe8..6f33b1a94 100644
--- a/lisp/doom-editor.el
+++ b/lisp/doom-editor.el
@@ -255,10 +255,10 @@ tell you about it. Very annoying. This prevents that."
 
 (use-package! autorevert
   ;; revert buffers when their files/state have changed
-  :hook (focus-in . doom-auto-revert-buffers-h)
   :hook (after-save . doom-auto-revert-buffers-h)
   :hook (doom-switch-buffer . doom-auto-revert-buffer-h)
   :hook (doom-switch-window . doom-auto-revert-buffer-h)
+  :hook (doom-switch-frame . doom-auto-revert-buffers-h)
   :config
   (setq auto-revert-verbose t ; let us know when it happens
         auto-revert-use-notify nil
diff --git a/lisp/doom-ui.el b/lisp/doom-ui.el
index 7f8424347..52c4d6bbb 100644
--- a/lisp/doom-ui.el
+++ b/lisp/doom-ui.el
@@ -91,22 +91,60 @@ want to change your symbol font, use `doom-symbol-font'.")
   "A list of hooks run after changing the focused windows.")
 
 (defcustom doom-switch-frame-hook nil
-  "A list of hooks run after changing the focused frame.")
+  "A list of hooks run after changing the focused frame.
+
+This also serves as an analog for `focus-in-hook' or
+`after-focus-change-function', but also preforms debouncing (see
+`doom-switch-frame-hook-debounce-delay'). It's possible for this hook to be
+triggered multiple times (because there are edge cases where Emacs can have
+multiple frames focused at once).")
 
 (defun doom-run-switch-buffer-hooks-h (&optional _)
-  (let ((gc-cons-threshold most-positive-fixnum)
-        (inhibit-redisplay t))
+  "Trigger `doom-switch-buffer-hook' when selecting a new buffer."
+  (let ((gc-cons-threshold most-positive-fixnum))
     (run-hooks 'doom-switch-buffer-hook)))
 
-(defun doom-run-switch-window-or-frame-hooks-h (&optional _)
-  (let ((gc-cons-threshold most-positive-fixnum)
-        (inhibit-redisplay t))
-    (unless (equal (old-selected-frame) (selected-frame))
-      (run-hooks 'doom-switch-frame-hook))
-    (unless (or (minibufferp)
-                (equal (old-selected-window) (minibuffer-window)))
+(defun doom-run-switch-window-hooks-h (&optional _)
+  "Trigger `doom-switch-window-hook' when selecting a window in the same frame."
+  (unless (or (minibufferp)
+              (not (equal (old-selected-frame) (selected-frame)))
+              (equal (old-selected-window) (minibuffer-window)))
+    (let ((gc-cons-threshold most-positive-fixnum))
       (run-hooks 'doom-switch-window-hook))))
 
+(defvar doom-switch-frame-hook-debounce-delay 2.0
+  "The delay for which `doom-switch-frame-hook' won't trigger again.
+
+This exists to prevent switch-frame hooks getting triggered too aggressively due
+to misbehaving desktop environments, packages incorrectly frame switching in
+non-interactive code, or the user accidentally (and rapidly) un-and-refocusing
+the frame through some other means.")
+
+(defun doom--run-switch-frame-hooks-fn (_)
+  (remove-hook 'pre-redisplay-functions #'doom--run-switch-frame-hooks)
+  (let ((gc-cons-threshold most-positive-fixnum))
+    (dolist (fr (visible-frame-list))
+      (let ((state (frame-focus-state fr)))
+        (when (and state (not (eq state 'unknown)))
+          (let ((last-update (frame-parameter fr '+last-focus)))
+            (when (or (null last-update)
+                      (> (float-time (time-subtract (current-time) last-update))
+                         doom-switch-frame-hook-debounce-delay))
+              (with-selected-frame fr
+                (unwind-protect
+                    (run-hooks 'doom-switch-frame-hook)
+                  (set-frame-parameter fr '+last-focus (current-time)))))))))))
+
+(let (last-focus-state)
+  (defun doom-run-switch-frame-hooks-fn ()
+    "Trigger `doom-switch-frame-hook' once per frame focus change."
+    (let ((inhibit-redisplay t))
+      (or (equal last-focus-state
+                 (setq last-focus-state
+                       (mapcar #'frame-focus-state (frame-list))))
+          ;; Defer until next redisplay
+          (add-hook 'pre-redisplay-functions #'doom--run-switch-frame-hooks-fn)))))
+
 (defun doom-protect-fallback-buffer-h ()
   "Don't kill the scratch buffer. Meant for `kill-buffer-query-functions'."
   (not (eq (current-buffer) (doom-fallback-buffer))))
@@ -669,9 +707,9 @@ triggering hooks during startup."
   ;; Make `next-buffer', `other-buffer', etc. ignore unreal buffers.
   (push '(buffer-predicate . doom-buffer-frame-predicate) default-frame-alist)
 
-  ;; Initialize `doom-switch-window-hook' and `doom-switch-frame-hook'
-  (add-hook 'window-selection-change-functions #'doom-run-switch-window-or-frame-hooks-h)
-  ;; Initialize `doom-switch-buffer-hook'
+  ;; Initialize `doom-switch-*-hook' hooks.
+  (add-function :after after-focus-change-function #'doom-run-switch-frame-hooks-fn)
+  (add-hook 'window-selection-change-functions #'doom-run-switch-window-hooks-h)
   (add-hook 'window-buffer-change-functions #'doom-run-switch-buffer-hooks-h)
   ;; `window-buffer-change-functions' doesn't trigger for files visited via the server.
   (add-hook 'server-visit-hook #'doom-run-switch-buffer-hooks-h))
diff --git a/modules/tools/magit/config.el b/modules/tools/magit/config.el
index 5f4231f31..d60e73510 100644
--- a/modules/tools/magit/config.el
+++ b/modules/tools/magit/config.el
@@ -50,7 +50,7 @@ Only has an effect in GUI Emacs.")
   ;; ...then refresh the rest only when we switch to them or refocus the active
   ;; frame, not all at once.
   (add-hook 'doom-switch-buffer-hook #'+magit-revert-buffer-maybe-h)
-  (add-hook 'focus-in-hook #'+magit-mark-stale-buffers-h)
+  (add-hook 'doom-switch-frame-hook #'+magit-mark-stale-buffers-h)
 
   ;; The default location for git-credential-cache is in
   ;; ~/.cache/git/credential. However, if ~/.git-credential-cache/ exists, then
diff --git a/modules/ui/modeline/+light.el b/modules/ui/modeline/+light.el
index dacff3b7f..41d67b2f2 100644
--- a/modules/ui/modeline/+light.el
+++ b/modules/ui/modeline/+light.el
@@ -368,7 +368,7 @@ Requires `anzu', also `evil-anzu' if using `evil-mode' for compatibility with
              ;; In case the user saves the file to a new location
              after-save-hook
              ;; ...or makes external changes then returns to Emacs
-             focus-in-hook
+             doom-switch-frame-hook
              ;; ...or when we change the current project!
              projectile-after-switch-project-hook
              ;; ...when the visited file changes (e.g. it's renamed)
diff --git a/modules/ui/vc-gutter/config.el b/modules/ui/vc-gutter/config.el
index 13eba6aad..9f6e08df2 100644
--- a/modules/ui/vc-gutter/config.el
+++ b/modules/ui/vc-gutter/config.el
@@ -118,8 +118,9 @@ Respects `diff-hl-disable-on-remote'."
           :n "{" #'diff-hl-show-hunk-previous
           :n "}" #'diff-hl-show-hunk-next
           :n "S" #'diff-hl-show-hunk-stage-hunk))
-  ;; UX: Refresh gutter on ESC or refocusing the Emacs frame.
-  (add-hook! '(doom-escape-hook doom-switch-window-hook) :append
+  ;; UX: Refresh gutter in the selected buffer on ESC, switching windows, or
+  ;;   refocusing the frame.
+  (add-hook! '(doom-escape-hook doom-switch-window-hook doom-switch-frame-hook) :append
     (defun +vc-gutter-update-h (&rest _)
       "Return nil to prevent shadowing other `doom-escape-hook' hooks."
       (ignore (or inhibit-redisplay