US President Donald Trump on Tuesday , the man who leads the agency charged with investigating his campaign's ties with Russia -- a move that sent shockwaves through Washington.
The surprise dismissal of Comey, who played a controversial role in last year's presidential election, came as he was leading a probe into whether Trump's aides colluded with Moscow to sway the November vote.
WATCH: Kellyanne Conway defends Trump's decision
Top Senate Democrat Chuck Schumer said he told Trump he was making a "big mistake" by dismissing Comey, a move that prompted parallels with a decision by a crisis-plagued Richard Nixon to fire his attorney general.
Trump "has accepted the recommendation of the attorney general and the deputy attorney general regarding the dismissal of the director of the Federal Bureau of Investigation," his spokesman Sean Spicer told reporters.
A search for a new FBI director was to begin "immediately," the White House said.
In a letter, Trump told Comey: "You are hereby terminated and removed from office, effective immediately."
"While I greatly appreciate you informing me, on three separate occasions, that I am not under investigation, I nevertheless concur with the judgment of the Department of Justice that you are not able to effectively lead the Bureau."
"It is essential that we find new leadership for the FBI that restores public trust and confidence in its vital law enforcement mission," Trump said.
The stated reason for Comey's dismissal -- according to a memo from Deputy Attorney General Rod Rosenstein that was circulated by the White House -- was for mishandling the probe into Democratic presidential hopeful Hillary Clinton's emails.
But his sacking raised immediate questions about Trump's motives.
FBI directors are appointed for a single 10-year term. The 56-year-old Comey, who is popular among rank-and-file agents, was appointed four years ago.
He played an outsized -- and controversial -- role on the American political stage over the past year, lobbing one bombshell after another that rankled both parties in Washington.
Clinton accused Comey of trashing her chances of becoming president by revealing an renewed investigation into her email use.
Comey told lawmakers last week he felt "mildly nauseous" at the thought that he had swayed the election -- but could not have acted any other way.
WATCH: Comey 'nauseous' at thought he swayed US election
'Nothing less than Nixonian'
Since the start of Trump's presidency, the FBI chief had increasingly appeared to be a thorn in the president's side.
He has confirmed that the agency is investigating Russian interference in last year's presidential election and notably Moscow's possible collusion with Trump's campaign.
Democrats -- already angry that Congressional inquiries into Russian meddling have been hamstrung by Republicans' willingness to defend Trump -- voiced sharp concerns that the FBI's investigation may now be in jeopardy too, with several calling for an independent commission to take over the probe.
"This is nothing less than Nixonian," charged Senator Patrick Leahy of Vermont, who called Trump's official justification for firing Comey "absurd."
"That fig leaf explanation seeks to cover the undeniable truth: The president has removed the sitting FBI director in the midst of one of the most critical national security investigations in the history of our country -- one that implicates senior officials in the Trump campaign and administration," he charged.
When Trump initially decided to keep Comey -- who was appointed by Barack Obama -- in his job, it raised eyebrows from critics who saw it as a tacit reward for his role in damaging Clinton's chances.
But within months, the FBI chief was back in the national spotlight -- this time taking aim at Trump.
During testimony to Congress last month, Comey flatly rejected Trump's explosive claim that he was wiretapped by his predecessor.
Comey's public testimony -- watched by millions around the world -- came as Trump sought to steer the news focus by calling the question of Russian election meddling "fake news."
But it had become increasingly clear that Comey had set his sights on the issue of Russia's election meddling, which has stalked Trump's presidency since he took office.
