While Democrats uniformly condemned Trump's decision and demanded an independent investigation, the public reaction among the Republican majority in Congress was more mixed - and cautious.
Until now, most Republicans have rejected the idea of an independent commission or special prosecutor to investigate the potential links between Trump's campaign and Russia. Much will depend on whether Republicans in Congress are finally ready to confront the Trump White House over the Russia imbroglio, and whether voters in their districts will demand a tougher response.
Trump's move shocked and dismayed members on both sides of the aisle, and raised the possibility that more Republicans could back an independent probe, though for now the GOP leadership in the Senate seems to be digging in its heels.
Congressional aides, bleary-eyed and exhausted after having worked through most of the night, told Foreign Policy that at least four Democratic members of the Senate intelligence committee and one Republican, Senator John Cornyn, were not informed by the White House in advance of the decision.
The usually taciturn and reserved Republican chairman of the Senate Intelligence Committee - and Trump ally during the campaign - Senator Richard Burr, said he was "troubled by the timing and reasoning of Director Comey's termination," and called Comey's dismissal "a loss for the Bureau and the nation".
Burr's committee has already requested documents from Trump's associates to examine possible connections to Russia, a signal that the panel could be prepared to issue subpoenas to get ahold of those documents.
The committee also has asked the Treasury Department's foreign intelligence unit for any relevant documents related to Trump and his team, including any indications of possible money laundering.
Senator John McCain said he was "disappointed" at Comey's firing, Senator Ben Sasse called the timing of the firing "very troubling," and Senator Jeff Flake said: "I've spent the last several hours trying to find an acceptable rationale for the timing of Comey's firing. I just can't do it."
Still, most Republicans held their fire. They accused Democrats of hypocrisy, as they had previously blasted Comey over his handling of Hillary Clinton's emails during the campaign, before the FBI chief ever confirmed that Trump's Russia ties had been under investigation since mid last year. Senate Majority Leader Mitch McConnell defended Comey's firing and dismissed demands for an independent investigation beyond the twin congressional probes already underway.
2 Will the FBI and the Justice Department investigate or capitulate?
Comey was reportedly fired just days after requesting more resources and manpower for the Russia investigation. The question now is whether the next FBI director that Trump appoints will provide the resources needed for a rigorous, independent inquiry, or whether the new director will curry favour with the White House by seeking to undercut the investigation.
The same question applies more broadly to the civil servants and prosecutors at the Justice Department carrying out the counterintelligence probe, and whether they will follow the facts wherever they lead despite political pressure from the White House.
The President has sent a clear signal to back off and has repeatedly castigated the inquiry as a waste of time and money, repeatedly dismissing the consensus findings of the U.S. intelligence community as "fake news".
By tradition and by law, the FBI and the Justice Department are supposed to operate above and apart from partisan political influence, and to conduct investigations without fear or favour. Nixon tried but ultimately failed to block investigations into his Administration.
3 Who will run the FBI?
With Comey out, the logical choice to lead the FBI until a permanent director is selected would be Andrew McCabe, the current deputy director. But the Administration indicated today that it has other plans, underscoring how the White House wants to maintain tighter control of the bureau. Officials are reportedly reviewing choices other than McCabe for the interim director job.
As for a permanent director, some names have popped up as possible candidates for the job. Speculation focused on Ray Kelly, the former New York City police commissioner who managed the force following the attacks of September 11, 2001, and Congressman Trey Gowdy, a former federal prosecutor who criticised Comey for failing to recommend an indictment against Hillary Clinton for her use of a private email server while Secretary of State. (Gowdy held a series of exhaustive hearings into Clinton's role in the death of Americans at a diplomatic compound in Libya in 2012, but ultimately found no evidence of any wrongdoing by the former Secretary of State). Whoever gets the nomination, the Senate confirmation hearings will be highly-charged and hard-fought.
Comey is the first FBI Director to be fired since 1993, when President Bill Clinton sacked William Sessions, whom the inspector general found had committed numerous ethical violations.
Now that he is out of office, Comey will also face a decision on whether to speak out publicly about what he knows, and whether he believes the White House is trying to squelch the Russia investigation.
Senator John Warner, the ranking Democrat on the Senate Intelligence Committee, told reporters that he had invited Comey to appear in a closed-door session before the committee next Wednesday.
"I think Jim Comey has got to have - if not his day in court, at least his day on the Hill," Warner said.
4 Will Flynn "flip" against the Trump Team?
Comey's dismissal came just as the investigation into Russia's ties to Trump aides appeared to be gaining momentum.
Federal prosecutors have issued grand jury subpoenas to associates of former national security adviser Michael Flynn, requesting business records, CNN reported.
The subpoenas from the US Attorney's Office in Alexandria, Virginia, targeted associates who worked with Flynn on contracts after he was forced out as director of the Defence Intelligence Agency in 2014. (Flynn, fired this year as National Security Adviser after less than a month in the job for lying about his pre-inauguration contacts with Russian officials, also worked as an agent for the Turkish Government during the campaign without registering as such with the Justice Department.)
Legal experts have speculated that Flynn, who faces potential prosecution if he is found to have lied to FBI investigators, could at some point "flip" and offer prosecutors damaging evidence against Trump's team in a potential deal to lessen any prison sentence.
Sally Yates, the former acting Attorney-General sacked by Trump earlier this year, told Congress on Tuesday that she discussed possible charges against Flynn with the White House counsel. But it's still unclear if Flynn will ultimately be charged.
- Foreign Policy