In 1653, three men from Oyster Bay, Richard Holbrook, Robert Williams and Daniel Whitehead, purchased a parcel of land from the Matinecock tribe.

[3] The arrival of the Long Island Rail Road in 1867 transformed the economy of Huntington from primarily agriculture and shipping (based on its well protected harbor) to tourism and commuting.

[3] The end of World War II brought about an explosive growth of population in Huntington as western Suffolk County began suburbanizing.

[3] Farms and resorts gave way to homes, and Huntington transformed into a major commuter town for nearby New York City.

[3] In 1988, the Supreme Court ruled that Huntington had violated the Fair Housing Act by preventing apartment construction anywhere except in black neighborhoods.

[5] The Supreme Court ordered the town to build an affordable housing project in a white neighborhood.

[4] In 2023, a council member proposed legalizing basement apartments to alleviate the housing crisis in Huntington and other communities surrounding New York City.

[4] At a July 2023 hearing, in which local residents railed against "migrants, pedophiles, or criminals" moving into Huntington, council members backtracked on their support for the zoning change.

[4] Huntington is bounded by Long Island Sound to the north, Nassau County to the west, Babylon to the south, and Smithtown to the east.

The town clerk position is held by Andrew Raia,[20] and the highway superintendent is Andre Sorentino,[21] both Republicans.

[24] Around 2002, Swiss International Air Lines's North American headquarters moved from Melville to Uniondale, Town of Hempstead.

[25][26] In 1997, Aer Lingus announced that it was moving its North American headquarters from Manhattan to Melville; James Lyndon, a spokesperson for the airline, said that the company moved to Long Island in an effort to reduce costs, as leasing costs are lower on Long Island than in Manhattan.

The Long Island Rail Road's Port Jefferson Branch serves the town's vicinity, and uses stations between Cold Spring Harbor through Northport.

Huntington is the only township in the United States to ban self-service gas stations at the township level and among the few places in the U.S. where full-service gas stations are compulsory and no self-service is allowed;[66] the entire state of New Jersey and the western-Mid Valley portion of Oregon are the only other places in the country with similar laws.