"After a thorough legal review of the matter, Attorney General Herring has concluded that Virginia's current ban is in violation of the U.S. constitution and he will not defend it," spokesman Michael Kelly wrote.
Herring, a Democrat who campaigned in part on marriage equality, was to file a brief Thursday with the federal court in Norfolk, where one of the lawsuits is being heard, as notification of the state's change in position in the case, Kelly said.
The state's shift comes on the heels of court rulings in which federal judges struck down gay marriage bans in Utah and Oklahoma.
The lawsuits in Virginia say the state's ban violates the Constitution's equal protection and due process clauses.
The decision by Herring drew divided responses — celebration from attorneys challenging the ban and condemnation from conservative activists.
Tom Shuttleworth, representing the couples challenging the ban in Norfolk, praised Herring's position "on the basic human right of being able to marry the person of your choice."
"It's a nice day to be an American from Virginia," he wrote in an email.
But the conservative Family Foundation of Virginia called the development "disappointing and frightening."
Herring's announcement comes less than one month after Democrats who swept the top three offices in the state took office.
With the election of Democrats Terry McAuliffe as governor and Herring as attorney general, Virginia made a hairpin turn away from the socially conservative officeholders they succeeded, particularly Republican Attorney General Ken Cuccinelli, an activist on social issues such as abortion and gay marriage. McAuliffe issued an executive order on inauguration day prohibiting discrimination against state employees who are gay.
Virginia voters approved the same-sex marriage ban 57 percent to 43 percent in 2006. 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 survey's margin of error was plus or minus 3.1 percentage points.
It is not the first time an attorney general has decided to stop defending their state's gay marriage ban. In Pennsylvania, Attorney General Kathleen Kane said last year that she would stop defending that state's gay marriage ban, also calling it unconstitutional. An outside law firm was hired to represent the state in a lawsuit over the ban.
Proponents of striking down 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 had been 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.
The legal costs in the Norfolk case are being paid for by the American Foundation for Equal Rights, which was behind the effort to overturn California's gay marriage ban.
David Boies and Theodore B. Olson, the high-profile legal tandem that brought down California's prohibition on same-sex marriage, lead the legal team in that challenge. Both cited Virginia's history when they announced their challenge.
"This case is about state laws that violate personal freedoms, are unnecessary government intrusions, and cause serious harm to loving gay and lesbian couples," Olson had said.
The Norfolk lawsuit's plaintiffs are two couples: Timothy Bostic and Tony London, and Carol Schall and Mary Townley. Bostic and London applied for a marriage license with the Norfolk Circuit Court Clerk's office in July 2013, but their application was denied.
Bostic and Schall were legally married in California in 2008. They have a daughter, whom Schall gave birth to in 1998, but Bostic can't adopt her because Virginia law doesn't allow same-sex couples to adopt children, according to the lawsuit.
The lawsuit argues that Virginia law stigmatizes gay men and lesbians, along with their children and families, because it denies them the same definition of marriage afforded to opposite-sex couples.
In that state General Assembly, Democratic legislators are still widely outnumbered in the House of Delegates, but they have been emboldened by the shift away from a reliably conservative state. They took immediate aim at the state's ban on gay marriage, but proposed constitutional amendments face a long road. The earliest voters could see a proposed amendment is in 2016.
There are currently 17 states that allow gay marriage.