The town was formed in 1813 from the Town of Windham, but was then called "Edwardsville." The name of "Hunter" was assumed in 1814. Afterwards, the town lost some territory to the Town of Saugerties in 1814 and to the Town of Jewett in 1849.
The area became a popular tourism destination in the late 19th and early 20th centuries. It was serviced by the Ulster and Delaware Railroad which brought tourists to resort towns throughout the Catskill Mountains.