I think you're spot on, modest can't handle that due to the silly pathnames it uses for the cache (~/.modest/cache/mail/imap/$USERNAME__$SERVER_$PORT). Which is also why it doesn't allow changing the account settings after it's connected once.

Possible workarounds might be to use the IP address instead of the hostname for one of the accounts, or set one up as IMAP with STARTTLS on port 143 and the other as IMAPS on port 993 (assuming the server supports this).