The change takes effect September 1.
Other states to have allowed gay marriage are Connecticut, Iowa and Massachusetts, but their decisions were made by the states' top courts.
Homosexual rights group the National Gay and Lesbian Task Force hailed Vermont's vote as "a momentous day and significant turning point in the struggle for the equal treatment of our relationships."
"We salute the courage and commitment of the Vermont state legislative leadership in pursuing this measure's passage -- even successfully overriding the governor's veto," the group said in a statement.
Former Vermont governor Madeleine Kunin expressed "elation" at the assembly's revolt.
"The grass roots support that was evident in today's vote signifies strong support for equal rights for our gay and lesbian relatives, friends and neighbors to a degree that has not happened before," she wrote on The Huffington Post website.
In addition to the four states allowing same-sex marriage, nine others grant some of the legal benefits of marriage to gay couples through civil unions or domestic partnership laws.
Vermont's decision comes just days after a ruling by the Iowa Supreme Court to strike down a ban on gay marriage.
In a unanimous opinion, the court ruled that the state's ban on gay marriage "violates the equal protection clause of the Iowa Constitution."
California, meanwhile, remains locked in a bitter legal battle between pro- and anti-gay marriage camps.
The Supreme Court in San Francisco legalized gay marriage in a landmark ruling last May, but in November voters passed a change to California's constitution that redefined marriage as a union between a man and woman.
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