The town encompasses five distinct villages, each of which has its own post office. These constituent villages are Dennis (including North Dennis), Dennis Port, East Dennis, South Dennis, and West Dennis.
Dennis was first settled in 1639, by John Crowe (later Crowell) and Thomas Howes, as part of the town of Yarmouth. The town officially separated and incorporated in 1793. It was named after resident minister, Rev. Josiah Dennis. There was not enough land for farming, so seafaring became the town's major industry in its early history, centered around the Shiverick Shipyard.
Currently, Dennis is a popular seaside resort town, notable for its stately colonial mansions along the northern Cape Cod Bay coastline, and its picturesque, warm-water beaches along the southern Nantucket Sound.
The Cape Playhouse, in northern Dennis, is one of the oldest summer theatres in the United States (it is not clear which theatre is the oldest, as many make this claim), and among the best known. The actress Bette Davis was "discovered" while working there as an usher. Other famous Dennis residents include the author Mary Higgins Clark and actress Amy Jo Johnson, who grew up in Dennis.