Deputy Secretary Bill Burns admitted the months-long investigation into the September assault on the US mission in Benghazi, Libya, had taken "a clear-eyed look at serious, systemic problems, which are unacceptable."
He told reporters the department had "learned some very hard and painful lessons in Benghazi," where four Americans, including ambassador Chris Stevens, were killed in an attack by dozens of armed militants linked to Al-Qaeda.
Secretary of State Hillary Clinton and the whole department "take responsibility" for the issues highlighted by the Accountability Review Board (ARB) and accepted all of its 29 recommendations, he stressed.
But top Republican lawmaker Ileana Ros-Lehtinen said the panel made it clear in their 39-page report that a lack of leadership and management "is to blame for the series of errors that resulted in the loss of life.
"The recent resignations of three State Department officials is not the end, as the administration must continue to be held accountable," said Ros-Lehtinen, chairwoman of the House foreign affairs committee.
Clinton, who had to pull out of this week's scheduled congressional hearings due to illness, must "answer for these failures," she added in a statement.
US television networks said Assistant Secretary Eric Boswell, head of the bureau of diplomatic security, and Charlene Lamb, deputy assistant secretary for international programs, had stepped down, citing unnamed officials.
The third person to submit their resignation was not identified. State Department officials would not immediately confirm the reports to AFP.
Only hours earlier the panel blamed "systemic failures and leadership and management deficiencies at senior levels" in the bureaus of diplomatic security and Near Eastern affairs for "grossly inadequate" security in Benghazi.
"Frankly, the State Department had not given Benghazi the security, both physical and personnel, resources it needed," ARB chairman veteran diplomat Thomas Pickering told reporters, after briefing lawmakers early Wednesday on a classified section of the report.
Incoming Republican House committee chairman Ed Royce said after the briefing that he was "not surprised at all that these three State Department officials have resigned."
"In this day and age, with radical ideologies and weapons spreading, there is no excuse for a leadership failure like this. It is simply unacceptable," he said in a statement.
Asked why the lessons learned from the twin embassy bombings in Africa in 1998 had failed to be fully applied, ARB vice chairman Admiral Mike Mullen said "the world has changed dramatically in this decade."
"I think we are in a much more difficult and challenging position with respect to meeting the needs to be out there and engage and doing so in a way that our people are very specifically secure."
Mullen also stressed that while Clinton has taken responsibility, as head of the department which deploys more than 60,000 people around the world, she had not been made aware of the specific security concerns in Benghazi.
Republican Senator Marco Rubio, who sits on the intelligence committee, insisted however Clinton's testimony was "indispensable to any effort to address this failure and put in place a process to ensure this never happens again."
The Benghazi attack also complicated President Barack Obama's plans for his second term cabinet, as his rumored top favorite to replace Clinton, the US envoy to the United Nations, Susan Rice, was forced to drop out of the running.
Rice had come under relentless Republican fire for saying, days after the assault, that, according to the best intelligence the available, it was triggered by a "spontaneous" protest outside the mission.
The ARB panel confirmed there had been no protest prior to the September 11 attack, nor was there any intelligence of a threat of any kind.
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