"It's time for the commonwealth to be on the right side of history and the right side of the law," newly elected Democrat Mark R. Herring said in a state that fiercely resisted school integration and interracial marriage in the 1950s and '60s.
Republicans accused Herring of shirking his duty to defend the state's laws after less than two weeks on the job, while gay rights activists exulted over the latest in a string of victories - this one in a conservative and usually hostile region of the country.
"It's a nice day to be an American from Virginia," Tom Shuttleworth, one of the lawyers challenging the ban, said in an email.
The move reflects the rise of a new Democratic leadership in Virginia and illustrates how rapidly the political and legal landscape on gay marriage in the U.S. is shifting.
Herring, as a state senator, supported Virginia's 2006 voter-approved constitutional amendment defining marriage as the union of a man and woman. But he said he decided after a "thorough legal review" that it is unconstitutional, and he will join gay couples in two federal lawsuits challenging the ban.
"I have now concluded that Virginia's ban on marriage between same sex couples violates the Fourteenth Amendment of the U.S. Constitution on two grounds: Marriage is a fundamental right being denied to some Virginians, and the ban unlawfully discriminates on the basis of both sexual orientation and gender," he said.
A federal judge will hear arguments in one of those lawsuits next week.
Herring stressed the ban will be enforced in the meantime, meaning clerks will continue to deny marriage licenses to same-sex couples.
In a movement that began with Massachusetts in 2004, 17 states and the District of Columbia now allow gay marriage, most of them clustered in the Northeast. None of them is in the old Confederacy.
In just the past five weeks, federal judges struck down gay marriage prohibitions in deeply conservative Utah and Oklahoma, but those rulings are on hold while they are appealed.
"It's enormously powerful that Virginia is taking this position," said gay rights advocate James Esseks, director of the LGBT Project for the American Civil Liberties Union. "It is a solid part of the South. This is not the Northeast. This is not California."
Richard Socarides, who was a senior policy adviser in the Clinton administration, called Herring's action "a tipping point."
"Virginia is now on the cutting edge of this," he said. "I think it's highly significant any time a state attorney general takes this position, but even more significant given the political makeup of the state is traditionally more conservative and now perhaps viewed as a swing state."
Herring, whose Republican predecessor Ken Cuccinelli opposed gay marriage and abortion, was part of a Democratic sweep of the state's top three offices in November. Virginia's densely populated northern suburbs near Washington, D.C., are solidly Democratic, while other sections of the state remain solidly conservative Republican.
Gov. Terry McAuliffe, who led the Democratic slate of victories, said through a spokesman that he supports Herring.
But Victoria Cobb, president of the conservative Family Foundation of Virginia, said: "It's frightening that politicians like the attorney general feel that they can pick and choose which aspects of the Constitution they deem worthy to defend and apply."
The Republican speaker of the Virginia House accused Herring of setting a "dangerous precedent." State GOP chairman Pat Mullins said Herring should resign if he doesn't want to do his duty. And Republican state Delegate Todd Gilbert proposed a bill that would allow legislators to defend state laws when the attorney general refuses to do so.
It is not the first time an attorney general has decided to stop defending a state's gay marriage ban. In Pennsylvania, Democratic Attorney General Kathleen Kane did so last year, and the state has hired an outside law firm to argue its case.
Virginia voters approved their state's ban 57 percent to 43 percent. But a Quinnipiac University poll in July found that 50 percent of registered Virginia voters support same-sex marriage, while 43 percent oppose it. The margin of error was plus or minus 3.1 percentage points.
Opponents of the state's ban say the issue resonates in Virginia in particular because of a landmark 1967 U.S. Supreme Court decision involving a Virginia couple and interracial marriage.
Mildred and Richard Loving were married in Washington, D.C., and were living in Virginia when police raided their home in 1958 and charged them with violating the state's Racial Integrity law. They were convicted but prevailed before the Supreme Court.
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