Brad,
Don't know if this helps but I have run across things like this when a reference to an invalid column is made somewhere in the code. We have an NVO print routine that uses Datastores to retrieve data. This routine expects certain columns to exist but customers can customize it. If they remove a certain column then the routine stops working but no message is diplayed - it then leaves the app in a very odd state. Windows can close but ItemChanged doesn't fire and other things.
When you say it continues painting properly are you able to open new windows in your App? Is the problem just on the window that the response came from? You mentioned 'at some point on the response window' what is happening there? Is it a real response window or one that you have popped up in a 'modal' state? Do you have reference pointers there?
Chris Craft