"Any decisions at any level not to defend individual laws must be exceedingly rare," Holder said at a meeting of the top law enforcers' national association. "And they must never stem merely from policy or political disagreements hinging instead on firm constitutional grounds."
His own view, he said, is that "we must be suspicious of legal classifications based solely on sexual orientation."
The issue has been divisive at the state level, with some attorneys general declining to defend same-sex marriage bans when challenged in court. Others have stated publicly that they are sworn to uphold the laws of their state, whether or not they agree with them.
"I fear that refusing to defend unpopular or politically distasteful laws will ultimately weaken the legal and moral authority that attorneys general have earned and depend on," Colorado Attorney General John Suthers, a Republican, wrote in a Washington Post opinion column this month. "We will become viewed as simply one more player in a political system rather than as legal authorities in a legal system."
Democratic attorneys general in at least six states Virginia, Pennsylvania, California, Illinois, Oregon and Nevada have declined to defend same-sex marriage bans that have been challenged in court by gay couples.
The remarks come on the heels of a Justice Department announcement expanding more federal privileges to same-sex couples, with Holder saying weeks ago that same-sex spouses cannot be compelled to testify against each other, should be eligible to file for bankruptcy jointly and are entitled to the same rights and privileges as federal prison inmates in opposite-sex marriages.
Holder himself refused to defend the federal Defense of Marriage Act in 2011, which helped lead to last year's Supreme Court decision striking down a key part of that law that denied gay married couples the federal benefits and privileges enjoyed by heterosexual couples.
"As I've said before, this decision was not taken lightly. Our actions were motivated by the strong belief that all measures that distinguish among people based on their sexual orientation must be subjected to a heightened standard of scrutiny and, therefore, that this measure was unconstitutional discrimination," Holder said.
Mississippi Attorney General Jim Hood said after the speech that he respected that Holder "approached it in a mindset that reasonable legal minds can disagree on an issue, as to how we approach it."
Hood said he has not yet been asked to defend his state's ban on same-sex marriage, but has been watching the court fights in other states.
J.B. Van Hollen, the Republican attorney general of Wisconsin and president of the attorneys general association, disagreed with Holder, saying the job of any attorney general is to uphold, not challenge, their state's constitution.
"We are the ultimate defenders of our state constitutions not the United States attorney general or the attorney general from another state," he said, adding, "It is our duty and obligation to defend them, or no one else will."