Cool idea, unfortunately most people's knowledge on this topic is limited which is why I like the choice to leave the yellow box out. I only knew Chicago, but guessing got me to more than half the answers before I gave up. I actually started typing Bridgeport (I live in CT) but I thought it was too insignificant.
I grew up in the town that had the oldest flag in the country. It is the one that was carried in the revolutionary war. Maybe it should be included. I won't say what it was so that people reading the comments don't get a free answer :).