Just two weeks on the job, the newly elected Democrat said Thursday he would fight against Virginia's ban on same-sex marriage, angering Republicans and conservatives who accused him of abandoning his job.
"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," said Victoria Cobb, president of the Family Foundation of Virginia.
With Herring's decision, gay marriage moved closer to gaining its first foothold in the South and gay rights activists cheered the latest in a string of victories—this one in a conservative and usually hostile region of the country.
"It's time for the commonwealth to be on the right side of history and the right side of the law," Herring said of a state that fiercely resisted school integration and interracial marriage in the 1950s and '60s.
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.
He said marriage is a fundamental right and the ban unlawfully discriminates on the basis of sexual orientation and gender.
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 bans in deeply conservative Utah and Oklahoma, but those rulings are on hold while they are appealed.
Gay rights advocates said Herring's decision is an important gesture in the conservative South.
"It's enormously powerful that Virginia is taking this position," said 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 in the Washington, D.C., area 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.
State Republican chairman Pat Mullins said Herring should resign if he doesn't want to do his duty. And GOP state Delegate Todd Gilbert proposed a bill that would allow legislators to intervene in lawsuits and 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 an outside law firm has been hired by the state to defend the ban.
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.
Associated Press writers Alan Suderman in Richmond and Mark Sherman in Washington contributed to this report.
Steve Szkotak can be reached on Twitter at http://twitter.com/sszkotakap.