Nearby Lake Champlain was an important military and trade route during the colonial period. The lake and the town were named in honor of Samuel de Champlain, who first surveyed the area in 1609. It was part of Canada until 1763, and became part of the United States in 1783.
The town was formed in 1788, the same year the county was established. In 1799, the town was reduced by the formation of the Town of Chateaugay (now in Franklin County). The founding of the towns of Chazy and Mooers in 1804 further reduced Champlain.
Champlain is on the border with Canada and contains three border crossings: Champlain, Overton Corners, and Rouses Point. The Champlain Port of Entry on Interstate 87 is one of the four most important commercial gateways on the northern border, connecting Quebec Autoroute 15 from Montreal to New York City.