This bug does not seem to be related to the recent menu updates and is experienced even in GZDoom 3.7.2, for example, in the "Customize Controls" menu. In post-3.7.2, the bug can be demonstrated with the "Action Controls" menu instead. This bug only affects the way the menu is drawn, and does not let you actually select a non-existent item.
How to reproduce: go to the menu and press the up arrow key to switch to the last item. Note that there is empty space between the last item and the bottom of the screen:
This does not happen if you scroll down from the top with the down arrow key. The last item is always at the very bottom:
This particular issue always happens only when the ScrollTop value for the menu in question is greater than 0. For example, it does not manifest in the "Gameplay Options" menu (ScrollTop is 0).
The weirdest thing is how scrolling to the bottom of the menu with the mouse works. Sometimes it will allow you to scroll further beyond the last item's position and sometimes it won't. So far I haven't been able to find out why this happens. This doesn't seem to be related to the ScrollTop value (it happens in the gameplay menu as well) but it is still possible that these two problems are somehow related, which is why I'm making a single report for both. If it turns out these issues are unrelated, I will make another report for the second one.