Flushing's first European settlers arrived in the 1620's, naming it after the seacoast village of Vlissingen (meaning "running water") in their native Holland. The town's name was later anglicized to "Flushing".

Two days after Christmas in 1657, the town fathers of the fledgling community rejected Governor Peter Stuyvesant's demand that they expel "Quakers, Papists, Jews, and other heretics" in a letter now known as the Flushing Remonstrance. In so doing, Flushing became the first town in the Americas to guarantee religious freedom to all of its residents.

Traces of the early Dutch history of Vlissingen can still be found in modern Flushing today, such as the Bowne House (the second oldest house in New York), the Bowne Street Community Church and the Flushing Quaker Meeting House (the oldest house of worship in New York).

Throughout the 18th Century, the Flushing Friends Meeting House was at the forefront of the movement to secure freedom of conscience throughout the American colonies, and the Flushing Remonstrance was an important influence on the First Amendment to the Constitution of the United States.

In the 19th century, Flushing became a center of the abolitionist movement, and a major stop on the Underground Railroad for freed slaves.

Through the 20th century, Flushing's population grew to include thousands of European immigrants and African American artists migrating from the South. During the 1970's, sizeable numbers of East Asian immigrants began to settle in Flushing. By 2000, Asians and Asian-Americans comprised roughly 35% of the population.