The 3D viewport renders over the file browser(s), maybe pausing the viewport when dialogs open would be helpful
Though for the entity / object properties dialog you'll want to see your changes update the viewport...
The file browser now defaults to a Qt based browser on Linux, avoiding the bug, maybe in the future it will be possible to use the local browser.
Until then, we avoid the bug.
The 3D viewport renders over the file browser(s), maybe pausing the viewport when dialogs open would be helpful Though for the entity / object properties dialog you'll want to see your changes update the viewport...