"Maybe it is occurring when my computer has to restart at night for updates, "

You would not leave QB running all the time, though. When you change a Preference, that is saved in a .ini file (initialization).

"or when we connect to it remotely??"

Remotely doesn't mean you control everything about the Local computer. It depends on your connectivity tools, but the Preference setting and that .ini file is saved to the Local computer and for the Signed in User. So, sometimes, you are working in a connectivity that does not result in either a Saved .ini or an applied .ini.

Example:

Your local computer has the program and file, and you log in as Admin. I remote in and log in as User1. I do not get your screen settings. And I cannot Save them or change them or set mine, if the system cannot write a .ini file for me to that local computer. Remember that my computer doesn't even have to have QB installed, so there is no local .ini file for me.

"If I knew which preference file or registry key these settings were saved in"

Open that program. Use F2, then F3. Use the Open File tab. Here they all are.

"I could copy it out to my desktop and overwrite them when it gets screwed up..."

Be Careful. There is a lot more in .ini files than "I want this window on the left."