The former FBI director boldly challenged the president who fired him, accused the Trump administration of lying and supplied material that could be used to build a case against President Donald Trump.
But after stepping away from the Capitol Hill spotlight, where he's always seemed comfortable, the 56-year-old veteran lawman now confronts the same question long faced by Washington officials after their government service.
His dry quip at a riveting Senate hearing that he was "between opportunities" vastly understates the career prospects now available to him - not to mention potential benefits from the public's fascination with a man who has commanded respect while drawing outrage from both political parties.
Comey was pilloried for his handling of the Hillary Clinton email investigation, yet is now seen as a critical cog in the inquiry into possible connections between Russia and the Trump campaign. He may be called upon to provide more detail about his interactions with Trump, which he documented in a series of memos, even as he turns attention to potential opportunities in law, corporate work or perhaps even politics.
"There's some jobs where the controversy would not be a benefit, but that's why I see him ending up in a place where he can be himself," said Evan Barr, a former federal prosecutor in New York City who worked under Comey in the U.S. attorney's office. "If he were the president of a college or an important think tank, he could pursue the issues that mean the most to him and not be worried about trying to make anyone happy."
Comey is unlikely to play any sort of direct role in the investigation now led by special counsel Robert Mueller, his predecessor as FBI director. But he almost certainly would avail himself as a witness to Mueller in any obstruction of justice investigation centered on his firing, or to further discuss requests he received from Trump that he interpreted as directives.
Comey's carefully crafted memos are laden with contemporaneously recorded details and verbatim quotes that could easily lay down a path for investigators, and already have been turned over to Mueller. In one note, Comey says Trump cleared the room before encouraging Comey to end an investigation into Trump's national security adviser, Michael Flynn.
Comey's decision to share with reporters, through an intermediary, details from those conversations, and his insistence on testifying in public attest to his determination to confront the president head-on.
"I do think he is unquestionably, if this thing goes anywhere, one of the star witnesses," said Robert Anderson, a retired FBI executive assistant director. "It really comes down to his testimony, in some avenues."
Career options are generally plentiful for departing FBI leaders and attorneys general. Both Mueller and former Attorney General Eric Holder, for instance, took jobs with prestigious law firms after leaving public service.
But few if any have as public a profile as Comey or have generated such intense feelings.
Even Democrats who disagree with his firing remain stung by his revival of the Clinton email investigation days before the November election.
Pro-Trump Republicans who were pleased by Comey some seven months ago may now concur with the president's assessment of Comey as a "showboat."
And companies that do business with the government might find it risky to bring aboard someone who's so publicly at odds with the current administration.
Comey's name over the years has been floated in politics, though it's not clear the former Republican - now an independent - has any interest.
Educated at the College of William & Mary, where he wrote a senior thesis on a 20th century theologian, Comey went on to law school at the University of Chicago. The bulk of his work has been in government, with the exception of private practice legal work in Virginia early in his career, lucrative general counsel stints at defense contractor Lockheed Martin and a Connecticut hedge fund, and a teaching job at Columbia University.
He was the U.S. attorney in Manhattan who in 2003 charged Martha Stewart with obstructing justice in a stock trade investigation. He then became deputy attorney general, the No. 2 spot at the Justice Department, where he famously faced down fellow Bush administration officials over a surveillance program authorization. In 2013, he was sworn in as FBI director, a job he's called the honor of his life.
Friends and colleagues say the father of five reveled in his public service.
"Anyone who has ever worked with Jim as far as I know, certainly speaking for myself, holds him in incredibly high esteem," said Sharon McCarthy, who worked for him at the U.S. attorney's office. "You'd be working late, he'd have a Coke in his hand and he'd come in, sit down, put his feet on your desk and start talking,"
Though Comey joked at a Senate hearing one week before his May 9 firing that he perhaps regretted picking up the phone when he was recruited for the FBI job while living comfortably in Connecticut, he also was known to pepper speeches with cracks about the "soulless" private sector.
He'd urge young audiences to imagine asking themselves on their death beds who they would want to have been, saying he hoped everyone's answer would be that they tried to help others.
His own law firm life, he'd say, was lacking despite the matching furniture, parking space and Colonial-style home that accompanied the job.
"You do not make much money working for the FBI. You will not get famous working for the FBI. But you will be rich beyond belief if you look at it from [the public service] vantage point," he has said.
One other question for Comey regardless of his next job will be how much he chooses, either directly or through intermediaries, to respond to allegations from Trump or Republicans rallying to the president's defense. On Friday, Trump strongly suggested Comey had lied about their encounters and accused him of being a "leaker."
"In the days to come," Comey friend Ben Wittes wrote on his Lawfare blog, "we're going to see a full-court press against Comey; indeed it is already well under way."