Hmmm... I don't go to Destin very often, but when I do, we always hit Red Bar, AJ's, Howl at the Moon and Hog's Breath. There's usually a fair amount of Locals hanging out at all of those places on the weekends. Not sure about week nights. Plus, I'm sure there are some new bars that have opened recently that I don't know about. They tend to draw local crowds as they open.
I have a few friends that have lived in Destin and may have more suggestions. I'll email them and see what they say.
If you make it in to Criolla's (in Grayton) anytime soon, ask for the Tim, the General Manager. He's a good friend and has lived in Destin and Panama City and would be more than happy to help you out. Tell him Steve from TripSmarter sent you. He may even have some suggestions for local hangouts in the Grayton/Seaside area.
I'll try and help with your
Panama City question, too...