The decision came with important caveats, and sweeping change will not happen overnight for women, nearly 300,000 of whom have deployed to Iraq and Afghanistan since 2001.
But the move by Defense Secretary Leon Panetta, with the support of President Barack Obama, could open 237,000 positions to women in America's armed forces and an expand opportunities for career advancement.
"The department's goal in rescinding the rule is to ensure that the mission is met with the best-qualified and most capable people, regardless of gender," Panetta said in a statement.
A senior defense official said Panetta's goal "is to open everything" to women. Service chiefs will have to ask for exceptions to keep some positions closed.
Panetta, who is to address a Pentagon news conference on Thursday, made the decision after the Joint Chiefs of Staff concluded it was time to integrate women "to the maximum extent possible," according to a statement.
Gender-neutral performance standards will be developed for all the new jobs opening to women, officials said. But whether that means the physical requirements become more or less rigorous remains to be seen, they added, cautioning that they would depend on the actual demands of the position.
An example of a physically demanding job that may be out of reach of women without significant upper body strength could be in front-line tanks, where soldiers need to lift and load heavy ammunition in confined spaces using mainly their arms.
A US official, speaking on condition of anonymity, said the changes would be gradual. The service chiefs have until May 15 to offer plans to implement the new policy by January 1, 2016.
"The secretary understands with a change of this magnitude it does take some time," the official said.
The move topples another societal barrier in the US armed forces, after the Pentagon in 2011 scrapped its "Don't Ask, Don't Tell" ban on gays and lesbians serving openly in the military.
The American Civil Liberties Union, which filed a suit in November seeking to force the Pentagon to end the ban on women in combat, applauded the decision, which rescinds a 1994 policy preventing women from serving in small front-line combat units.
For many women service members, the move is belated acknowledgement of the realities of the past decade of war, in which there were often no clearly defined front lines. Eighty-four women have been killed in hostile action in Iraq and Afghanistan and nearly 1,000 wounded.
Women serve in combat roles for the armed forces of a few developed nations, including Canada and Israel, but officials say demand from women for such jobs in NATO nations is very low. In 2010, Britain decided after a review that it would not change rules excluding women from infantry or combat teams.
"I feel like it's beyond time," said Staff Sergeant Tiffany Evans, a soldier stationed at Fort Hood, Texas.
The United States is drawing down its some 66,000 remaining forces from Afghanistan through the end of 2014, when only a small residual force is expected to remain. It is possible that some women may see themselves in new combat roles before that withdrawal is complete.
"I don't think we can exclude that possibility," one senior defense official said, speaking on condition of anonymity.