Rice has since said she deeply regrets the U.S. inaction in Rwanda. She moved from the NSC to the State Department during President Clinton's second term, serving as the Assistant Secretary of State for African Affairs, one of the youngest people to ever to hold the position.
When President George W. Bush took office, Rice left the State Department for Brookings. In 2007, she joined the first Obama presidential campaign as Senior Adviser for National Security Affairs. Rice was a staunch, outspoken surrogate for the president, and according to her detractors, maybe too outspoken.
In a 2008 Huffington Post blog, she sharply criticized Obama's primary opponent, then-Sen. Clinton, for voting for the Iraq war, saying it proved Clinton wouldn't be ready for a "3 a.m. call" in a national security emergency.
"Senators Clinton and McCain failed the judgment test when they voted for George Bush's Iraq war -- a war which has made America less safe and is the greatest strategic blunder of our generation -- without even bothering to read the full National Intelligence Estimate."
Rice was accused of being ageist in her later criticism of Sen. John McCain, calling him "confused" over the war in Iraq in a conference call with reporters.
"A real disturbing, even disconcerting pattern of confusing the basic facts and reality that pertain to Iraq from John McCain over a series of months. He doesn't know how many forces we have there. He thought we were down to pre-surge levels," Rice said.
Her loyalty and blunt-speaking manner has been appreciated and rewarded by allies, such as Albright and President Obama. When he took office he named Rice as the U.S. Permanent Representative to the United Nations.
But those same qualities have also made her a divisive figure in Washington. Some Washington insiders have wondered whether Rice -- Benghazi aside -- is the right person to be America's top diplomat.
"By all accounts, she is talented, capable and extremely abrasive," Washington Post political reporter Dana Milbank told ABC News. "Does she have the temperament to be the nation's top diplomatic? She's very smart, very driven, not necessarily very diplomatic."
William Antholis, the Managing Director of the Brookings Institute, worked closely with Rice at both Brookings and in the Clinton administration. Antholis told ABC News via email that few people in Washington rival Rice's knowledge and understanding of both foreign affairs and political institutions.