The bombshell announcement that sent shock and surprise ricocheting through Washington ends the career of the man who was once seen as the unimpeachable and nonpartisan ideal of how a law enforcement officer should behave. But Comey saw his reputation tarnished when he was dragged into the toxic politics of the 2016 campaign.
In recent days, he again came under fire for his handling of the investigation into Hillary Clinton's private email server. Many Democrats believe that his announcement that he was re-opening the probe 11 days before the election cost the former secretary of state the presidency.
The Trump administration said his dismissal was the direct result of his handling of the Clinton probe.
But Democrats rejected that notion, immediately raising comparisons to the Watergate era and claiming that the FBI chief was fired because his investigation got too close to the White House.
The Trump administration, however, said Comey was fired based on the clear recommendations of both Deputy Attorney General Rod Rosenstein and Attorney General Jeff Sessions. Sessions has recused himself from the Russia investigation since he was a member of Trump's campaign team.
In a signed letter, Trump informed Comey that he was "hereby terminated and removed from office, effective immediately," explaining that he reached the conclusion that Comey is "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 told Comey in the letter. "I wish you the best of luck in your future endeavors."
In a separate letter, rich in irony, Rosenstein laid out the reasons for Comey's firing, arguing that it was his transgressions over the Clinton email investigation that were the cause of his dismissal.
Senior White House officials did not think the firing would be a big political explosion, a source with knowledge of discussions inside the White House told CNN's Dana Bash. The thinking was that because Democrats were saying precisely what Rosenstein said in his letter and that there wouldn't be a backlash.
What was not thought through, apparently, was finding an answer to why now.
At the center of Rosenstein's rationale for recommending Comey's firing was the director's handling of the investigation into Clinton's private server, namely his decision to recommend no charges be filed and the news conference he held to explain his reasoning.
Rosenstein accused Comey of attempting to "usurp the attorney general's authority" by publicly announcing why he felt the case should be closed without prosecution.
"Compounding the error, the director ignored another longstanding principle: We do not hold press conferences to release derogatory information about the subject of a declined criminal investigation," Rosenstein argued in his memo.
"We should reject the departure and return to the traditions (of the bureau)," Rosenstein said. "The way the director handled the conclusion of the email investigation was wrong. As a result, the FBI is unlikely to regain public and congressional trust until it has a director who understands the gravity of the mistakes and pledges never to repeat them."
But Senate Democratic minority leader Chuck Schumer said he told Trump on the telephone that he had made a terrible mistake.
"Were these investigations getting too close to home for the President?" Schumer asked.
CNN's senior legal analyst Jeffrey Toobin, was also not buying the idea that Comey was sacked over the Clinton investigation, saying it was "absurd."
Toobin branded the move a "grotesque abuse of power by the President of the United States."
"This is not something that is within the American political tradition," Toobin said, comparing the sacking of Comey to President Richard Nixon's firing of special prospector Archibald Cox during the Watergate scandal.
"This is not normal. This is not politics as usual," Toobin said though added that Trump did have the legal authority to fire an FBI director.
The White House however said that the impetus for the firing of Comey came from Rosenstein, noting that he was a career prosecutor who served under President Barack Obama as the US Attorney for Maryland, and was confirmed in his new job on April 25.
A senior administration official said that Rosenstein assessed the situation upon taking office and concluded the FBI director had lost his confidence. He sent his recommendation to Sessions who forwarded it to Trump, who accepted it on Tuesday.
But former officials of the Clinton campaign, accused Trump of using the furor over Comey's handling of the email server as a ruse to get out from under the Russia investigation.
"I was as frustrated, concerned and disappointed as anyone with Director Comey's handling of the email investigation, but President Trump just fired the man investigating how Russia meddled in our election and whether members of his campaign were involved, an investigation President Trump called "charade" only 24 hours ago," said Clinton's former campaign manager Robby Mook.
"It's equally concerning that our attorney general, who lied about his own meetings with the Russians, approved Director Comey's firing," he said.
One Trump loyalist, who worked on the campaign and the transition gave his reaction to CNN's Jim Scuitto.
"I firmly believe the Russia angle is fake news. But this gives me pause," the person said.
Senior Justice and FBI officials say they were unaware of the Comey decision until the announcement. Officials who spoke to CNN said they are shocked by the development.
Comey's term was due to run until 2023. The decade-long tenure was introduced to shield FBI directors from being drawn into politics.
The firing of Comey sent shockwaves through Capitol Hill.
Sen. Lindsey Graham, who is leading one of four investigations into Russia's interference in the election, said he supported Trump's decision.
"Given the recent controversies surrounding the director, I believe a fresh start will serve the FBI and the nation well," Graham said in a statement Tuesday. "I encourage the President to select the most qualified professional available who will serve our nation's interests."
But Democrats, like Pennsylvania Sen. Bob Casey blasted the move.
"This is Nixonian. Deputy Attorney General Rod Rosenstein must immediately appoint a special counsel to continue the Trump/Russia investigation," he said.
While Democrats renewed their demands for a special counsel, arguing that the Trump Justice Department could not be trusted to oversee the case, Republicans insisted that one was not needed.
"I think Rod Rosenstein, the new deputy attorney general is competent to lead that effort," said Texas Sen. Joh Cornyn, a member of the GOP leadership.
But Republican Senate Foreign Relations Committee Chairman Bob Corker said that though Rosenstein's rationale for removing Comey was sound, it, would "raise questions."
"It is essential that ongoing investigations are fulsome and free of political interference until their completion, and it is imperative that President Trump nominate a well-respected and qualified individual to lead the bureau at this critical time," Corker said in a statement.
And Sen. John McCain added: "While the President has the legal authority to remove the director of the FBI, I am disappointed in the President's decision to remove James Comey from office."
The Arizona senator renewed his request for a special congressional committee to review the Russia allegations.
Comey's last appearance on Capitol Hill last week exacerbated doubts about his position. Just before news of his dismissal broke aiming to clear up his statement that former Clinton aide Huma Abedin "forwarded hundreds and thousands" of emails to her husband's laptop.
The note, signed by Gregory Brower, assistant director of the FBI's Office of Congressional Affairs, clarified that the "hundreds and thousands of emails" that Comey said were 'forwarded" from Abedin to her husband's email "included emails transferred via backups as well as manual forwarding."
The White House said it will immediately launch the search for a new FBI director.
Comey was appointed FBI director by President Barack Obama in 2013.
In so doing, he elevated a Republican law enforcement veteran who had been critical of the Justice Department under former President George W. Bush to the top domestic investigative and surveillance organization, among the most powerful posts in the world.
In the decades since former FBI Director J Edgar Hoover, the controversial director who brought FBI into the modern era, law enforcement has avoided the appearance of influencing politics the way Hoover did.
But Comey's decision to thrust himself repeatedly into the 2016 election, put him at odds with the FBI's general decision to stay away from the political spotlight.
Comey made the decision in July to go public with his recommendation that the Justice Department not pursue any charges against former Secretary of State Hillary Clinton or her former staffers over her email practices as secretary of state. However, he also took the opportunity to rebuke Clinton at length as being "extremely careless" with sensitive information.
Then-candidate Trump had talked up the investigation until this point, at which time he and his campaign derided Comey for the "political" decision.
Just days away from the election, Comey jumped into the race again. He informed Congress, via letter, that the FBI had re-opened its investigation into Clinton. The decision was made because of its investigation into former Rep. Anthony Weiner, who is married to Clinton confidant Huma Abedin. Comey followed up days later with another letter, informing Congress that the FBI didn't find anything and continued to believe Clinton's practices did not merit the pursuance of any criminal charges.
After Clinton's loss, former President Bill Clinton blamed Comey for it, as have many Clinton staffers, at least in part.
After taking office, Trump met with Comey at the White House.
He offered a cryptic remark to the FBI chief.
"Oh, here's Jim," Trump said in January. "He's become more famous than me."
By Stephen Collinson, Jeff Zeleny and Jeremy Diamond, CNN
CNN's Sara Murray, Ted Barrett, Eli Watkins, Shimon Prokupecz and Scott Glover contributed to this report.