Internal Server Error (500) can be caused by many many different things, and it is very difficult to just “guess” what might be causing the problem on your site.
It would help if you explained more about your site:
What comprises your site? (do you have only static html and/or graphics)
Are you running CGI scripts, and if so what scripts?
What do your error logs (found at /home/yourusername/log/yourdomainname/) show when the error occurs?
The 404 error is a natural result of the 500 error if an error page cannot be found, and it will likely be resolved when you fix the 500 error.