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The town was founded in 1640, when settlers from Lynn, Massachusetts, established residence on lands obtained from local Shinnecock Indian Nation. The first settlers included eight men, one woman, and a boy who came ashore at Conscience Point. These men were Thomas Halsey, Edward Howell, Edmond Farrington, Allen Bread, Edmund Needham, Abraham Pierson the Elder, Thomas Sayre, Josiah Stanborough, George Welbe, Henry Walton and Job Sayre. By July 7, 1640, they had determined the town boundaries. During the next few years (1640-43), Southampton gained another 43 families; there are now thousands of people in Southampton.

From 1644, the colonists established an organised whale fishery, significant in the history of whaling as the first in New England. They chased pilot whales (“blackfish”) onto the shelving beaches for slaughter, a sort of dolphin drive hunting. They also processed drift whales they found on shore. They observed the Native Americans’ hunting techniques, improved on their weapons and boats, and then went out to ocean hunting.

The first meeting house was on a hill that is the site of the current Southampton Hospital. The town’s oldest existent house is the Halsey House at 249 Main Street, which was built by Thomas Halsey, one of the first Englishmen to trade with the Shinnecocks.