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Dutch settlers derived the name of the town from limestone that used to lie on the shore of the river according to a popular tradition. This tradition is supported by 17th century wills and deeds, which may be found in The New York Genealogical and Biographical Record, that refer to “the white stone” as a local landmark and survey reference point. Whitestone got its name because the settlers discovered that Whitestone was built on white limestone.

The area was, in large part, the estate of Francis Lewis, a delegate to the Continental Congress and a signer of the Declaration of Independence. The estate was the site of an English raid during the Revolutionary War. Lewis was not present but his wife was taken prisoner and his house was burned to the ground. For a period of time Whitestone was called Clintonville after Dewitt Clinton, the former governor of New York; this etymology is present in the name of Clintonville Street, located in the neighborhood. In the late 19th century, many wealthy New Yorkers began building mansions in the area, on what had once been farmland or woodland. Rapid development of the area ensued in the 1920s, however, as trolley and Long Island Rail Road train service on the Whitestone Branch was expanded into the neighborhood. Although this rail service ended during the Great Depression, part of the right-of-way was later used by Robert Moses to help construct the Belt Parkway, which includes the Whitestone Expressway which runs along the southeast edge of the former Flushing Airport and through Whitestone. Flushing Airport has been abandoned since 1985.

Further development came with the building of the Bronx-Whitestone Bridge in 1939. The bridge measures 2,300 feet and was the fourth longest bridge in the world at the time of its construction.