Gay and lesbian couples already could marry in 36 states and the District of Columbia. The court's 5-4 ruling means the remaining 14 states, in the South and Midwest, will have to stop enforcing their bans on same-sex marriage.
"No union is more profound than marriage," wrote Justice Anthony Kennedy, joined by the court's four more liberal justices. The vote comes just weeks after Ireland became the first country to legalize gay marriage via referendum.
Hundreds of activists gathered outside the Supreme Court building Friday to celebrate the decision, chanting, "Love has won" and singing the US national anthem. The crowd also raised a large flag with the pink equal sign that has come to symbolize the gay marriage movement.
The four dissenting justices each filed a separate opinion explaining their views.
"This court is not a legislature. Whether same-sex marriage is a good idea should be of no concern to us," Chief Justice John Roberts wrote in dissent.
"If you are among the many Americans - of whatever sexual orientation - who favor expanding same-sex marriage, by all means celebrate today's decision," Roberts said. "But do not celebrate the Constitution. It had nothing to do with it."
President Barack Obama welcomed the decision via Twitter, calling it "a big step in our march toward equality."
The ruling will not take effect immediately because the court gives the losing side roughly three weeks to ask for reconsideration. But some state officials and county clerks might decide there is little risk in issuing marriage licenses to same-sex couples.
Today is a big step in our march toward equality. Gay and lesbian couples now have the right to marry, just like anyone else. #LoveWins— President Obama (@POTUS) June 26, 2015
The cases before the court involved laws from several states that define marriage as the union of a man and a woman. Those states have not allowed same-sex couples to marry within their borders and they also have refused to recognize valid marriages from elsewhere.
Just two years ago, the Supreme Court struck down part of the federal anti-gay marriage law that denied a range of government benefits to legally married same-sex couples.
The decision in that case did not address the validity of state marriage bans, but courts across the country, with few exceptions, said its logic compelled them to invalidate state laws that prohibited gay and lesbian couples from marrying.
The number of states allowing same-sex marriage has grown rapidly. As recently as October, just over one-third of the states permitted same-sex marriage.
There are an estimated 390,000 married same-sex couples in the United States, according to Williams Institute at the University of California, Los Angeles, which tracks the demographics of gay and lesbian Americans. Another 70,000 couples living in states that do not currently permit them to wed would get married in the next three years, the institute says. Roughly 1 million same-sex couples, married and unmarried, live together in the United States, the institute says.
The Obama administration backed the right of same-sex couples to marry. The Justice Department's decision to stop defending the federal anti-marriage law in 2011 was an important moment for gay rights and President Barack Obama declared his support for same-sex marriage in 2012.