The town was first settled circa 1812.
The town was formed in 1821 from the Town of Jay. At that time the town was called "Dansville." In 1822, the name was changed, as suggested by a settler from Vermont, to "Wilmington" due to confusion with another "Dansville" in New York. In 1848, part of the town was partitioned off to form the Town of St. Armand.
At the beginning of the 20th century, the tourist industry began to develop in the town.
"Santa's Workshop," one of the nation's first theme parks for children, is located near the community of North Pole. Whiteface Mountain (4,870 feet) was the site of alpine events for the 1932 and 1980 Winter Olympics.