The town of Dunkirk is split into two sections, east and west, by the city of Dunkirk, which is a separate entity.
The area was first settled around 1808. Development was slow until the New York and Erie Railroad established a station in Dunkirk village in 1851. The town of Dunkirk was established in 1859. The village of Dunkirk was incorporated in 1837, becoming a city in 1888.
The first naval skirmish in the War of 1812 began in Lake Erie near the mouth of Canadaway Creek, which is now within the boundaries of the western part of the town. A small marker commemorating the event sits near the intersection of Route 5 and Temple Street.