The town was founded in 1640,[3] when settlers from Lynn, Massachusetts, established residence on lands obtained from local Shinnecock Indian Nation.

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.

They chased pilot whales ("blackfish") onto the shelving beaches for slaughter, a sort of dolphin drive hunting.

[6] Southampton has 47 public and private cemeteries,[7] not including Shinnecock Hills Golf Club, which is claimed as an Indian burial ground that is no longer in active use.

In 2005, the Shinnecock Indian Nation filed a lawsuit against the state seeking the return of 3,500 acres (14 km2) in Southampton near the tribe's reservation, and billions of dollars in reparations for damages suffered by colonial land grabs.

The tribe challenged the state legislatures' approval of an 1859 sale of the 3,500 acres of tribal land.

The suit charged that in 1859, a group of powerful New York investors conspired to break the lease by sending the state Legislature a fraudulent petition from a number of Shinnecock tribal members.

[1] Southampton contains seven incorporated villages and 16 unincorporated areas, which are called hamlets in New York state.

In 2016, according to Business Insider, the 11962 zip code encompassing Sagaponack, within Southampton, was listed as the most expensive in the U.S., with a median home sale price of $8.5 million.

[19] Major employers in Southampton include[20] The town supervisor is Maria Z. Moore, a registered member of the Democratic Party, who was elected in November 2023 with 56.99% of the vote against Republican Cynthia Mc Namara.

The Town of Southampton is served primarily by Suffolk County Transit bus routes, although Hampton Jitney buses are available for trips to and from New York City.