diff --git a/popup.c b/popup.c
index fe34f2c0..2a543b6c 100644
--- a/popup.c
+++ b/popup.c
@@ -487,6 +487,8 @@ popup_key_cb(struct client *c, void *data, struct key_event *event)
 	size_t			 len;
 	u_int			 px, py, x;
 	enum { NONE, LEFT, RIGHT, TOP, BOTTOM } border = NONE;
+	struct window		*w;
+	struct window_pane	*wp;
 
 	if (pd->md != NULL) {
 		if (menu_key_cb(c, pd->md, event) == 1) {
@@ -505,14 +507,20 @@ popup_key_cb(struct client *c, void *data, struct key_event *event)
 			popup_handle_drag(c, pd, m);
 			goto out;
 		}
+		w = c->session->curw->window;
+		wp = w->active;
 		if (m->x < pd->px ||
 		    m->x > pd->px + pd->sx - 1 ||
 		    m->y < pd->py ||
 		    m->y > pd->py + pd->sy - 1) {
 			if (MOUSE_BUTTONS(m->b) == MOUSE_BUTTON_3)
 				goto menu;
+			wp->flags |= PANE_FOCUSED;
+			pd->flags &= ~POPUP_FOCUSED;
 			return (0);
 		}
+		wp->flags &= ~PANE_FOCUSED;
+		pd->flags |= POPUP_FOCUSED;
 		if (pd->border_lines != BOX_LINES_NONE) {
 			if (m->x == pd->px)
 				border = LEFT;
@@ -559,7 +567,8 @@ popup_key_cb(struct client *c, void *data, struct key_event *event)
 			bufferevent_write(job_get_event(pd->job), buf, len);
 			return (0);
 		}
-		input_key(&pd->s, job_get_event(pd->job), event->key);
+		if (pd->flags & POPUP_FOCUSED)
+			input_key(&pd->s, job_get_event(pd->job), event->key);
 	}
 	return (0);
 
@@ -723,6 +732,7 @@ popup_display(int flags, enum box_lines lines, struct cmdq_item *item, u_int px,
 
 	server_client_set_overlay(c, 0, popup_check_cb, popup_mode_cb,
 	    popup_draw_cb, popup_key_cb, popup_free_cb, popup_resize_cb, pd);
+	pd->flags |= POPUP_FOCUSED;
 	return (0);
 }
 
diff --git a/server-client.c b/server-client.c
index 9ced4482..6aed51e8 100644
--- a/server-client.c
+++ b/server-client.c
@@ -2595,6 +2595,8 @@ server_client_handle_key(struct client *c, struct key_event *event)
 {
 	struct session		*s = c->session;
 	struct cmdq_item	*item;
+	struct window_pane	*wp;
+	int			done;
 
 	/* Check the client is good to accept input. */
 	if (s == NULL || (c->flags & CLIENT_UNATTACHEDFLAGS))
@@ -2612,16 +2614,16 @@ server_client_handle_key(struct client *c, struct key_event *event)
 			status_message_clear(c);
 		}
 		if (c->overlay_key != NULL) {
-			switch (c->overlay_key(c, c->overlay_data, event)) {
-			case 0:
-				return (0);
-			case 1:
-				server_client_clear_overlay(c);
-				return (0);
+			done = c->overlay_key(c, c->overlay_data, event);
+			TAILQ_FOREACH(wp, &c->session->curw->window->panes, entry) {
+				if (wp->flags & PANE_FOCUSED)
+					goto focused;
 			}
+			if (done)
+				server_client_clear_overlay(c);
+			return (0);
 		}
-		server_client_clear_overlay(c);
-		if (c->prompt_string != NULL) {
+focused:	if (c->prompt_string != NULL) {
 			if (status_prompt_key(c, event->key) == 0)
 				return (0);
 		}
@@ -2893,7 +2895,7 @@ server_client_reset_state(struct client *c)
 	tty->flags &= ~TTY_BLOCK;
 
 	/* Get mode from overlay if any, else from screen. */
-	if (c->overlay_draw != NULL) {
+	if (c->overlay_draw != NULL && ~wp->flags & PANE_FOCUSED) {
 		if (c->overlay_mode != NULL)
 			s = c->overlay_mode(c, c->overlay_data, &cx, &cy);
 	} else if (c->prompt_string == NULL)
@@ -2924,7 +2926,7 @@ server_client_reset_state(struct client *c)
 				cy = tty->sy - n;
 		}
 		cx = c->prompt_cursor;
-	} else if (c->overlay_draw == NULL) {
+	} else if (c->overlay_draw == NULL || wp->flags & PANE_FOCUSED) {
 		cursor = 0;
 		tty_window_offset(tty, &ox, &oy, &sx, &sy);
 		if (wp->xoff + s->cx >= ox && wp->xoff + s->cx <= ox + sx &&
diff --git a/tmux.h b/tmux.h
index 480a22b2..722210da 100644
--- a/tmux.h
+++ b/tmux.h
@@ -3523,6 +3523,7 @@ int		 menu_key_cb(struct client *, void *, struct key_event *);
 #define POPUP_CLOSEEXIT 0x1
 #define POPUP_CLOSEEXITZERO 0x2
 #define POPUP_INTERNAL 0x4
+#define POPUP_FOCUSED 0x8
 typedef void (*popup_close_cb)(int, void *);
 typedef void (*popup_finish_edit_cb)(char *, size_t, void *);
 int		 popup_display(int, enum box_lines, struct cmdq_item *, u_int,