diff --git a/runtime/lua/vim/_extui/messages.lua b/runtime/lua/vim/_extui/messages.lua
index 5fc247020d..e791321383 100644
--- a/runtime/lua/vim/_extui/messages.lua
+++ b/runtime/lua/vim/_extui/messages.lua
@@ -491,9 +491,12 @@ function M.set_pos(type)
           return
         end
         vim.schedule(function()
-          api.nvim_win_set_config(win, save_config)
+          if api.nvim_win_is_valid(win) then
+            api.nvim_win_set_config(win, save_config)
+          end
           cmd_on_key = nil
           local entered = api.nvim_get_current_win() == win
+          ext.check_targets()
           -- Show or clear the message depending on if the pager was opened.
           if entered or not api.nvim_win_get_config(ext.wins.pager).hide then
             M.virt.msg[M.virt.idx.spill][1] = nil
@@ -502,6 +505,7 @@ function M.set_pos(type)
               api.nvim_command('norm! g<') -- User entered the cmdline window: open the pager.
             end
           elseif ext.cfg.msg.target == 'cmd' and ext.cmd.level <= 0 then
+            ext.check_targets()
             set_virttext('msg')
           end
           api.nvim__redraw({ flush = true }) -- NOTE: redundant unless cmdline was opened.
diff --git a/test/functional/ui/messages2_spec.lua b/test/functional/ui/messages2_spec.lua
index b5306d1b07..1fe45fb98a 100644
--- a/test/functional/ui/messages2_spec.lua
+++ b/test/functional/ui/messages2_spec.lua
@@ -217,4 +217,21 @@ describe('messages2', function()
       {9:E354: Invalid register name: '^@'}                    |
     ]])
   end)
+
+  it('hit-enter prompt does not error for invalid window #35095', function()
+    command('echo "foo\nbar"')
+    screen:expect([[
+      ^                                                     |
+      {1:~                                                    }|*10
+      {3:─────────────────────────────────────────────────────}|
+      foo                                                  |
+      bar                                                  |
+    ]])
+    feed('<C-w>o')
+    screen:expect([[
+      ^                                                     |
+      {1:~                                                    }|*12
+      foo [+1]                                             |
+    ]])
+  end)
 end)