The region, once called "Palmertown," was first settled around 1764. The Town of Wilton was created in 1818 from the Town of Northumberland. The Grant Cottage State Historic Site is located in Wilton, in an area known as Mount McGregor, which is the highest peak of the Palmertown Range, mostly north of Wilton. This site is the place where Ulysses S. Grant died in 1885 while completing his memoirs.

A narrow-gauge railway built in 1882, the Saratoga, Mount McGregor and Lake George Railroad, ran through Wilton.

• Ballard Corners – A hamlet by the east town line on NY-50 at the junction of County Road 33.
• Barnes Corners – A location in the southeast part of the town on NY-50.
• Dimmick Corners – A location in the northeast part of the town on County Road 32.
• Gurn Spring – A hamlet southeast of Wilton village on County Road 33.
• Kings Station – A hamlet south of Wilton village on US-9.
• Loughberry Lake – A small lake in the southwest part of Wilton.
• Mt. McGregor Correctional Facility – A New York state medium security prison at the north town line. On its grounds lies the Grant Cottage.
• Travers Corners – A hamlet south of Wilton village.
• Wilton – The hamlet of Wilton in located on US-9 at the junction with County Roads 101, 32, 33, and 34, in the north part of the town.

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