The statement from Press Secretary Sean Spicer said Comey was terminated and removed from office on the recommendations of Deputy Attorney General Rod Rosenstein and Attorney General Jeff Sessions.
"The FBI is one of our nation's most cherished and respected institutions, and today will mark a new beginning for our crown jewel of law enforcement," Trump said in a statement.
The search for a new permanent director will begin immediately, the White House said. The acting FBI Director is Andrew McCabe, who was until an hour ago Comey's deputy. Attorney General Sessions is expected to appoint an interim acting FBI Director in the coming days as the search for a permanent replacement continues.
In a letter to Comey, Trump said the firing was necessary to restore "public trust and confidence" in the FBI. Comey has come under intense scrutiny in recent months for his role in an investigation into Democrat Hillary Clinton's email practices, including a pair of letters he sent to Congress on the matter in the closing days of last year's election.
Trump made no mention of Comey's role in the Clinton investigation, which she has blamed in part for the election result that put him in the White House. But in announcing the firing, the White House circulated a scathing memo, written by deputy Attorney General Rod Rosenstein, criticizing Comey's handling of the Clinton probe, including the director's decision to hold a news conference announcing its findings and releasing "derogatory information" about Clinton.
The president asserted Comey informed him "on three separate occasions that I am not under investigation."
CLICK HERE to read the letters from President Trump, Attorney General Sessions and Deputy AG Rod Rosenstein
Comey was leading the investigation into Russia's interference in the 2016 presidential election and whether they had contact with anyone in the Trump campaign. The White House announced Tuesday night that Trump will meet with Russia's Minister of Foreign Affairs Wednesday morning.
House Democrats have asked top law enforcement officials to locate and secure materials and documents related to the FBI's Russia investigation and Trump's firing of Comey, and keep them off limits from White House officials and Attorney General Sessions. They also asked for any files related to Comey's firing to be preserved for review by members of Congress and any future investigations.
Tuesday's stunning announcement came shortly after the FBI corrected a sentence in Comey's sworn testimony on Capitol Hill last week. Comey told lawmakers that Huma Abedin, a top aide to Hillary Clinton, had sent "hundreds and thousands" of emails to her husband's laptop, including some with classified information.
On Tuesday, the FBI said in a two-page letter to the Senate Judiciary Committee that only "a small number" of the thousands of emails found on the laptop had been forwarded there while most had simply been backed up from electronic devices. Most of the email chains on the laptop containing classified information were not the result of forwarding, the FBI said.
Since Attorney General Jeff Sessions recused himself from the bureau's Trump-Russia probe, Rosenstein, his deputy, has been in charge.
This is only the second firing of an FBI director in history. President Bill Clinton dismissed William Sessions amid allegations of ethical lapses in 1993.
Democrats slammed Trump's action, comparing it to President Richard Nixon's "Saturday Night Massacre" decision to fire the independent special prosecutor overseeing the Watergate investigation in 1973, which prompted the resignations of the Justice Department's top two officials.
"This is Nixonian," Sen. Bob Casey, D-Pa., declared on Twitter. "Outrageous," said Oregon Sen. Ron Wyden, calling for Comey to immediately be summoned to testify to Congress about the status of the Trump-Russia investigation. Rep. Adam Schiff of California, top Democrat on the House intelligence committee, said the White House was "brazenly interfering" in the probe.
Senate Intelligence Committee Chairman Richard Burr (R-NC) released a statement, saying, "I am troubled by the timing and reasoning of Director Comey's termination. I have found Director Comey to be a public servant of the highest order, and his dismissal further confuses an already difficult investigation by the Committee. In my interactions with the Director and with the Bureau under his leadership, he and the FBI have always been straightforward with our Committee. Director Comey has been more forthcoming with information than any FBI Director I can recall in my tenure on the congressional intelligence committees. His dismissal, I believe, is a loss for the Bureau and the nation."
Sen. John McCain (R-Ariz.) said, "Well I regret that that action had to be taken. It's unfortunate because I think he's a good man. But the president does have that authority... I always believe that we should have a select committee or commission because it's a very large issue - it's gotten larger - and it'll get more large as time goes by."
Sen. Dick Durbin, the No. 2 Democrat in the Senate, stood on the Senate floor and said he would await word from the White House on whether the investigation will continue.
Durbin also released a statement, saying, "The termination and removal of James Comey as director of the Federal Bureau of Investigation raises the critical question as to whether the FBI investigation of Russian interference in the last presidential campaign will continue and as to whether the investigation of any collusion or involvement by the Trump campaign will also be investigated by the FBI. Any attempt to stop or undermine this FBI investigation would raise grave constitutional issues. Under these circumstances, I renew my call for an independent counsel and a special commission to fully investigate the Russian interference. We await clarification by the White House as soon as possible as to whether this investigation will continue and whether it will have a credible leader so that we know it will have a just outcome."
Illinois Sen. Tammy Duckworth released a statement, saying, "The President's actions transcend any one individual and raise significant concerns over the basic rule of law, especially if they are intended to dissuade criminal investigators from digging too deep into Trump Administration officials and associates - or even the President himself. If any doubts remained about the need for a transparent, impartial and independent investigation into the Trump Administration, the firing of Director Comey surely eliminates them. It is not clear why Attorney General Sessions, who previously claimed he would recuse himself from all Russia-related matters, was involved in firing the law enforcement official leading the Russia investigation. There are simply too many questions raised by tonight's actions, and the American people deserve nothing less than answers from an independent investigator."
Illinois Rep. Mike Quigly (D-5) released a statement, saying in part, "Today, President Trump added to his long record of disruption and distraction by attempting to hand select the individual that leads the investigation into his own Administration. It is no coincidence that Director Comey was fired shortly after confirming the existence of the FBI's investigation into collusion between the Trump campaign and Russian officials. Despite the Administration's illogical excuses, this move serves only one purpose: to stall the process and prevent the truth from being revealed to the American people. It is a brazen decision taken straight out of the Nixon playbook. We also can't ignore that this shocking decision was made in part on the recommendation of Attorney General Jeff Session who has recused himself from any investigations into collusion with Russia. The firing of Director Comey underscores two things: the need for a special prosecutor and the importance of our investigation in the House, as we continue our efforts to shine a light on information that this Administration is clearly trying to keep in the dark."
House Intel Cmte member @RepMikeQuigley on Comey firing: "de facto obstruction of justice."— Eric Horng (@EricHorngABC7) May 10, 2017
Senate Majority Leader Chuck Schumer (D-NY) said he told Trump he was making a "big mistake" by firing Comey as it would continue to raise suspicions about the Trump administration attempting to purge the Justice Department of the officials investigating Russia's interference with the 2016 election.
"We know the FBI has been looking into whether the Trump campaign colluded with the Russians, a very serious offense. Were these investigations getting too close to home for the president?" Schumer said. "This is part of a troubling pattern from the Trump Administration. They fired Sally Yates. They fired Preet Bharara. And now they fired Director Comey, the very man leading the investigation. This does not seem to be a coincidence."
Schumer called on Deputy AG Rosenstein to appoint a special prosecutor to continue the investigation.
Rep. Elijah Cummings (D-Md.), ranking member on the House Oversight Committee, said in part, "Congress needs to have immediate emergency hearings to obtain testimony directly from Attorney General Sessions, the deputy attorney general, and FBI Director Comey. The White House was already covering up for Michael Flynn by refusing to provide a single document to Congress, and now the President fired the one independent person who was doing the most to investigate President Trump and his campaign over allegations of coordination with Russia. It is mindboggling that the Attorney General - who claimed to have recused himself - was directly involved in the decision to fire Director Comey according to the White House itself. There is now a crisis of confidence at the Justice Department, and President Trump is not being held accountable because House Republicans refuse to work with us to do our job."
Rep. Eric Swalwell (D-Calif.), ranking member on the CIA subcommittee of the House Intelligence Committee, released a statement saying, in part, "The administration of justice must remain free of political influence, and President Trump has just leaped over that line. If he thinks this will halt or even slow investigations into his and his associates' conduct, he is sadly mistaken. The American people deserve to know what happened, and Trump's 'Tuesday Afternoon Massacre' won't interfere. Nobody recommended by this administration can be trusted to oversee this investigation, and so the need for an independent bipartisan commission is now more urgent than ever."
Whistleblower Edward Snowden also weighed in on Comey's firing on Twitter, saying that even though Comey has been trying to jail him for years, "If I can oppose his firing, so can you."
This FBI Director has sought for years to jail me on account of my political activities. If I can oppose his firing, so can you. https://t.co/zUp5kquy8q— Edward Snowden (@Snowden) May 9, 2017
Some lawmakers in both parties welcomed news of the dismissal, an indication of the broad concern in Washington surrounding Comey's tenure at the FBI.
"Given the recent controversies surrounding the director, I believe a fresh start will serve the FBI and the nation well," said Republican Lindsay Graham of South Carolina, chairman of a Senate Judiciary subcommittee investigating Russian interference in the 2016 presidential election.
Sen. Dianne Feinstein of California, the top Democrat on the Judiciary Committee, said Trump called her Tuesday afternoon to inform her of his decision.
"The next FBI director must be strong and independent and will receive a fair hearing in the Judiciary Committee," she said in a statement.
The FBI Agents Association President Thomas O'Connor released a statement on Comey's firing, saying:
"A change in FBI leadership of this magnitude must be handled carefully and with an eye towards ensuring that the Bureau can continue to fulfill its responsibility to protect the American public from criminal and national security threats.
We greatly appreciate Director Comey's service, leadership, and support for Special Agents during his tenure. He understood the centrality of the Agent to the Bureau's mission, recognizing that Agents put their lives on the line every day. His focus was to ensure that the Bureau's investigations complied with the law and the Constitution, and that Agents performed their mission with integrity and professionalism.
As vital stakeholders, FBI Agents should be given a voice in the process of selecting the next Director."
Comey has been at the center of election-related controversy since he publicly announced the FBI would not recommend prosecuting the-presidential candidate Hillary Clinton over emails found on a private server in a nationally-broadcast press conference.
Comey captured headlines again in October 2016 when he publicly announced that the investigation into Clinton's emails had been reopened, before saying no actionable items had been found a short time later. Analysts and Clinton herself have said they believe those announcements contributed to her election loss.
Less than a week before the election, Sen. Schumer said he had lost faith in Comey. "I do not have confidence in him any longer," he told Bloomberg News at the time.
In January, House Democrats left a briefing on Russian hacking furious, and calling Comey unfit to lead the FBI.
"I was nonjudgmental until the last 15 minutes. I no longer have that confidence in him," Rep. Tim Walz (D-Minn.), ranking member of the Veteran Affairs Committee, told The Hill. "Some of the things that were revealed in this classified briefing - my confidence has been shook."
That same day, the Wall Street Journal editorial board called on Comey to resign, saying, "The best service Mr. Comey can render his country now is to resign. Failing that, Jeff Sessions should invite him for a meeting after he is confirmed as Attorney General and ask him to resign."
And last week, Rep. Adam Schiff (D-Calif.) criticized Comey's "disparate" treatment of the Clinton email investigation and the investigation into Russian interference in the 2016 presidential election.
Clinton's advisers were stunned by Trump's decision Tuesday. Former campaign spokesman Brian Fallon said that while he believed Comey had "inflicted severe damage" on the FBI, "the timing and manner of this firing suggest that it is the product of Donald Trump feeling the heat on the ongoing Russia investigation and not a well thought out response to the inappropriate handling of the Clinton investigation."
"Nothing excuses the disparate way he handled those. I don't' think in any way he justified both what he did and why he treated those investigations so differently," Schiff said.
Comey, 56, is a 1985 graduate of the University of Chicago Law School and fondly remembered his time on Chicago's South Side in a speech at the University in October 2015.
"It's great to be back at the place I called home for three years," Comey told the crowd, urging students to consider a life of public service. "I didn't know exactly what I was going to do with my law degree but my hope was to find a job that would allow me to make a difference in some way. This school gave me the confidence and tools to serve people who needed help," he said.
He was nominated by President Barack Obama for the FBI post in 2013 to a 10-year term. Praised for his independence and integrity, Comey has spent three decades in law enforcement and has been no stranger to controversy.
Before the past months' controversies, Comey was perhaps best known for a remarkable 2004 standoff with top officials in the George W. Bush administration over a federal domestic surveillance program.
As the deputy attorney general, Comey rushed to the hospital bed of Attorney General John Ashcroft to physically stop White House officials in their bid to get his ailing boss to reauthorize a secret no-warrant wiretapping program.
Comey described the incident in 2007 testimony to Congress, explaining that he believed the spy program put in place after the Sept. 11, 2001, terror attacks was legally questionable.
When he learned that Andrew Card, the president's chief of staff, and Alberto Gonzales, the White House counsel, were heading to Ashcroft's hospital room despite Ashcroft's wife's instructions that there be no visitors, Comey told Congress, Comey beat them there and watched as Ashcroft turned them away.
"That night was probably the most difficult night of my professional life," Comey said.
Chuck Goudie, Barb Markoff, Christine Tressel, Ross Weidner and the ABC7 I-Team contributed to this report.
ABC News contributed to this report
The Associated Press contributed to this report.