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The land that is now Bellport was purchased along with what is now Brookhaven hamlet (then called Fireplace Neck) and western Southaven from the Unkechogue Indians in 1664 by settlers from nearby Setauket, who were attracted by the plentiful harvests of salt hay. The part which became Bellport was named Occumbomock Neck. Jonathan Rose was the first permanent settler in the 1680s, and by 1720, the Rose family owned much of Occumbomock Neck. In 1829, Thomas Bell moved there, envisioning a seaport, since Bellport was very close to the Old Inlet, a breach in the barrier island, Fire Island, which gave Bellport easy access to the open ocean. With Col. William Howell, he built a dock and road to the dock. The breach healed over, however, and Bellport instead became a tourist attraction, with wealthy visitors coming in by railroad and then coach from New York City. Although all seven of the hotels eventually closed, the last in the 1950s, Bellport remained associated with wealthy New Yorkers, who eventually established year-round residences. After World War 2, the nearby Camp Upton was converted into Brookhaven National Lab, bringing in more, highly educated, year-round residents.
Bellport was incorporated as a village in 1910. On July 4, 1980, the Bellport Academy and Bellport Village Historic District were listed on the National Register of Historic Places.
On March 8, 1963, Bellport High School burned down. No-one was killed, but 40 students and teachers were hospitalized. The replacement school was built in Brookhaven, but is still called Bellport High School.
On November 27, 1983, the New York Pyrotechnic Products Company factory (locally known as Grucci's), located just north of the village, exploded, killing two and injuring 24. The explosion had the effect of an earthquake, and caused significant damage to hundreds of homes.