With his highly public handling of the email probe and his resulting entanglement in the political tumult, Comey accomplished the unusual feat of antagonizing each side of the partisan divide. In the aftermath, his stature is diminished and his future in a Clinton or Donald Trump administration is highly uncertain.
Comey's new status as one of Washington's most polarizing leaders is a stunning twist for someone who long enjoyed the genuine respect of both parties. If he hoped his Sunday letter to lawmakers informing them that a review of new emails potentially tied to Clinton's server would quell the political storm swirling around him, he was mistaken.
Democrats pilloried him for influencing the final days of an already vitriolic campaign and Republicans accused him of caving to political pressure and questioned how the bureau could review thousands of emails so quickly.
"Right now, (Clinton) is being protected by a rigged system," Trump said at a rally
in Sterling Heights, Michigan.
"It's a totally rigged system. You can't review 650,000 emails in eight days. You can't do it folks," Trump said, mischaracterizing the number of emails the FBI was reviewing. Sources with knowledge of the investigation have told CNN the number is in the tens of thousands.
Dianne Feinstein, the top Democrat on the Senate Select Committee on Intelligence, said Comey "unfairly hurt the campaign of one candidate and changed the tenor of this election."
Can Comey continue?
Comey is three years into a 10-year appointment at the FBI. But there are now serious questions about whether his position is still tenable going forward — regardless of who becomes president.
By late Sunday, neither Clinton nor Trump supporters would definitively say their candidate still had confidence in Comey.
"It's not my place to come in and say if Director Comey is doing a good job or not a good job," Trump's senior communications adviser Jason Miller told CNN's Wolf Blitzer on "The Situation Room." "It is clear that the system is rigged. It is clear that this investigation has not been handled very well from the beginning."
Asked on "The Situation Room" whether he had confidence in Comey, Rep. Sean Duffy, a Trump supporter, said "I don't have any information from inside the FBI to make that conclusion right now."
Democratic Rep. G.K. Butterfield, a Clinton supporter, also refused to say whether he had confidence in the FBI chief.
"Director Comey has a good reputation and he's been a law enforcement professional for many years," Butterfield said.
Still, he expressed concern about the initial letter sent to Congress at the end of last month.
"I am still evaluating why he would send such a letter to Congress," Butterfield said.
Comey recognizes he's in a tough spot even after the election. But an official said he's given no indication he will resign.
FBI's reputation at stake
The FBI chief's future isn't all that's at stake. The political storm surrounding Clinton's emails and the FBI's handling of them threaten to tarnish the bureau itself.
Republicans are suspicious of the extent to which the FBI is being constrained by President Barack Obama's Justice Department. Democrats are worried that leaks and probes into the Clinton Foundation are indications that rank-and-file FBI agents are upset by Comey's decision not to seek indictments of Clinton.
Democratic vice presidential candidate Tim Kaine made a stunning charge Saturday that elements of the FBI were trying to throw the election to Trump -- a contention that would seemingly make it difficult for Comey to work in a Clinton administration.
"Comey knew that the FBI is not only a leaky sieve but there were people within the FBI actively working—actively working—to try to help the Trump campaign," Kaine said in an interview with Fusion. "This just absolutely staggering, and it is a massive blow to the integrity of the FBI."
From the start, the FBI probe into Clinton and Comey's handling of it has drawn him onto political ground anyone in his position would prefer to avoid. And it's been a reminder that once officials like Comey, who by definition required to be nonpartisan, enter the political crossfire, it's nearly impossible to get out with their character and prestige in place.
"The destruction of James Comey by political pressure is painful to watch," former House Speaker Newt Gingrich, tweeted on Sunday. "He is being twisted into an indefensible pretzel of contradictions."
If Clinton loses the election on Tuesday, Democrats are certain to blame Comey, since she saw her comfortable leads in opinion polls over Trump erode following his first letter to Congress just over a week ago.
If she wins, but her margin is narrow, or if Democrats fail to win back the Senate, Comey will also be accused of actions that had the effect of suppressing the Democratic vote and influencing the election.
"This should never have happened," Democratic Rep. Elijah Cummings said on "The Situation Room," arguing that Comey should never have sent the initial letter to Congress in the first place. "Unfortunately, Donald Trump and his associates have blown this thing up like Director Comey should have known."