His departure came just after reports surfaced the Justice Department warned the Trump administration last month that Flynn misled administration officials regarding his communications with the Russian ambassador to the United States and was potentially vulnerable to blackmail by the Russians.
"I inadvertently briefed the Vice President-elect and others with incomplete information regarding my phone calls with the Russian ambassador. I have sincerely apologized to the President and the Vice President, and they have accepted my apology," Flynn wrote according to a copy of his resignation letter obtained by CNN.
The Justice Department concern was raised after Flynn claimed he did not discuss with the Russian ambassador the sanctions being imposed by the Obama administration in retaliation for Russia's interference in the election. Flynn was not yet in government.
The message was delivered by then-Acting Attorney General Sally Yates. Other top intelligence officials, including James Clapper and John Brennan, were in agreement the White House should be alerted about the concerns.
The Washington Post
first reported the Justice Department message.
But Flynn was already in hot water. White House press secretary Sean Spicer issued a statement saying President Donald Trump is "evaluating the situation" around Flynn, who is in hot water after possibly misleading Vice President Mike Pence.
The issue stems from whether Flynn discussed sanctions against Russia with the Russian ambassador before Trump took office and then misled Pence about it. It created a turbulent 72 hours for the White House, leading to questions about Flynn's future after only three weeks.
"The President is evaluating the situation," Spicer's statement said. "He's speaking to the vice president relative to the conversation the vice president had with Gen. Flynn, and also speaking to various other people about what he considers the single most important subject there is: our national security."
The noncommittal statement came shortly after Kellyanne Conway, the counselor to the President, told reporters that Trump has "full confidence" in Flynn.
"Gen. Flynn does enjoy the full confidence of the President," Conway said on MSNBC. She later declined to detail how much the President knew about the issue and when he knew it, deeming those conversation private.
Many inside the Trump administration are concerned with the fact that the national security adviser could have misled senior members of the White House, including Pence, who went on television and denied that Flynn spoke about sanctions with Sergey Kislyak, Russian ambassador to Washington.
Trump, who particularly hates when aides generate negative press, has expressed displeasure with Flynn to aides in recent days, said a source close to the President. Trump and his team are particularly bothered by the possibility that Flynn misrepresented his conversations to Pence.
Flynn spoke with Pence at least twice Friday, according to another White House official who declined to say whether the conversations were about the ongoing controversy. The episode over sanctions against Russia has opened a rift between Flynn and Pence, who exchanged a chilly handshake Friday before Trump's news conference with Japanese Prime Minister Shinzo Abe.
Flynn also apologized to Pence and a source says the two "smoothed things over."
"The knives are out," the official added, acknowledging that Flynn's future in the White House is hardly a sure thing. "There's a lot of unhappiness about this."
Administration officials, some of who were once unsure about the details of the story, now believe the national security adviser did, in fact, discuss sanctions with the Russian ambassador. A US official confirmed to CNN on Friday that Flynn and Kislyak did speak about sanctions, among other matters, during a December call, contradicting past statements by White House officials.
After the call was made public, Pence told CBS News on January 15 that Flynn did not talk sanctions levied by the Obama administration with Kislyak.
"They did not discuss anything having to do with the United States' decision to expel diplomats or impose censure against Russia," Pence told CBS News.
On Friday, an aide close to the national security adviser told CNN that Flynn could not rule out that he spoke about sanctions on the call.
The White House official blamed much of the outcry against Flynn on a Washington culture that's always in search of a scalp, but people within Trump's orbit were unable to defend Flynn on Sunday.
Stephen Miller, White House policy director, was asked directly about Flynn's future on a number of Sunday talk shows. Miller responded by saying he was not the appropriate official to ask the question, hardly a ringing endorsement from the aide the Trump administration put out to talk on Sunday.
"I don't have any answers today," Miller said in response to questions about whether Flynn misled the vice president. "I don't have any information one way or another to add anything to the conversation."
New Jersey Gov. Chris Christie, a longtime Trump ally, told CNN's Jake Tapper Flynn needs to clear up his story with Trump and Pence in an interview Sunday on "State of the Union."
The White House official, pushing back against the idea that Flynn spoke about sanctions, raised questions about the uproar surrounding Flynn and poked holes in the criticism coming from the general's detractors.
Why, the official said, would a general with years of experience in the intelligence field jeopardize his career by discussing something he likely knew was being recorded.
Trump is also deeply loyal to Flynn: Their relationship stretches further back than many of the national security adviser's White House counterparts.
While Trump's top White House advisers like chief of staff Reince Priebus and chief strategist Steve Bannon only came aboard after Trump secured the Republican nomination, Flynn was an early supporter and joined Trump's campaign as his top foreign policy adviser in early 2016.
But Flynn was not just a policy adviser. He also played the role of top surrogate on the campaign trail, seeking to boost Trump's national security bona fides and also leading the charge on political attacks against Trump's Democratic rival Hillary Clinton.
Flynn was also a contender to join Trump on the Republican ticket as his running mate. But even after he wasn't tapped for the vice presidency, Flynn continued to travel with Trump to most of his political rallies as one of his most trusted advisers in his small circle of aides.
"It's a problem," a senior White House adviser said Friday about the possibility that Flynn misled Pence.