After you close the Kvatch gate the 'random' gates open 'randomly'

They don't depend on level, and just pop up from time to time. For example, I was playing a quest and one popped up just outside Bravil. I ended up loading a save prior to the gate that opened, did a few things differently, and when I went back to that spot, no gate was there.
You may close as many as you like, but it will take a very long time. I closed 4 or 5 before going main quest and closing the ones you need to close.