I think I figured it out... finally noticed this in the inspector:
This attempt to set a cookie via a set-cookie header was blocked because it was sent over an unsecure connection and would have overwritten a cookie with the Secure attribute
Out site is http://helpdesk/ and we were supposed to add SSL to it but had trouble when we launched so we figured it wasn't a big deal since it was only accessible internally.
I finally got the certificate working recently so we can use https://helpdesk/ but just haven't rolled it out since we have so many incomplete tickets.
Apparently, when I logon to https://helpdesk/ it saves the cookie, but then if I try http://helpdesk/ it fails the logon because I didn't keep the cookies it assigned me.
If I log out of the HTTPS site, the HTTP site works fine.
another contributing factor: some of the email templates use http://helpdesk/ but some have https://helpdesk/ which I'm guessing is why it came up randomly and not when I got the certificate installed