I’m certain that this is a bug that you are all experiencing. This never happens to me after pressing play and navigating the scene with an xBox/Windows controller.
I was able to reproduce part of this issue by focusing on the editor windows using mouse-click. After that, I can use the game controller to move focus from one window to another and even scroll up and down through the folder hierarchy but what happens there seems more random than anything else, I can’t actually access nested folders.
This doesn’t not affect me at all though once I’ve pressed “Play” The focus for my controller stays entirely within the active play area unless I specifically use the mouse to change focus to the Editor.
When using the controller to move around the various Editor areas, I can move up to the File drop-down menu and open it using the “A” button but I cannot move around in the drop-down menu nor can I activate any text entries or even close the menu once it’s been opened
This doesn’t seem at all like a feature, I’m sure it’s a bug and if it’s causing you any problems then you may want to consider filing a bug report so it can be fixed.