Hi Brian, this sounds like something that support would have a much better chance at solving for you than the community. I'd love to know how the Virtual Server is configured, whether there is cookie persistence (or other type of persistence) and what some of the other settings are like. The 500 Internal Server Error doesn't appear to me to be a timeout, so I'm a bit confused at what you mean by timeout.
Can you describe what happens? Are you just browsing inside the portal after being authenticated and then suddenly you receive a 500 Error? How many servers are in the pool behind the virtual? Do you get 500 errors even if you go to each instance on each server directly?
Nimbostratus