Dismissed by President Donald Trump in a shock announcement Tuesday, less than halfway into his 10-year term, Comey played a deeply controversial role in the run-up to last year's election - and beyond.
First, he hampered Hillary Clinton's White House bid with a damning assessment of her email practices as secretary of state - reopening the case days before the vote in a move the Democrat says cost her the election.
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When Trump decided to keep Comey - who was appointed by Barack Obama - in his job, it raised eyebrows from critics who saw it as a tacit reward for his role in damaging Clinton's chances.
But the FBI chief had increasingly appeared to be a thorn in the president's side.
Within months of the election, the 56-year-old was back in the national spotlight - this time taking aim at the sitting president, Trump, in a marathon hearing on the issue of Russia's alleged election meddling.
In the high-stakes March hearing followed live by millions around the world, Comey confirmed - for the first time - that his agency is investigating Moscow's alleged interference and, notably, its possible collusion with Trump's campaign.
He also flatly rejected Trump's explosive claim that he was wiretapped by his predecessor Obama.
Comey delivered his assessment without a blink, telling lawmakers that neither the Federal Bureau of Investigation nor the Justice Department had evidence to support such allegations.
Straight shooter
In his post at the FBI since September 2013, the towering Comey - he stands 6'8" (two meters) tall - is known as a highly-skilled political operator.
He has been circulating in political and legal circles at the highest level for three decades, which gave him the confidence to challenge the country's justice department, and even the White House.
Comey had set his sights firmly on the issue of Russia's alleged election meddling, which has stalked Trump's young presidency.
And if there is one character trait the FBI chief is known for, it is tenacity.
He locked horns relentlessly with Silicon Valley as he sought to convince Apple to unlock a smartphone used by the perpetrator of a terror attack in California. The FBI's own experts ended up breaking into the device.
The burning-hot Clinton investigation - which saw Comey assailed on all sides - did much to cement his reputation as a straight shooter, as well as thrust him into the public eye.
Independent
Many top US government careers begin in New York, and Comey is no exception - he hails from the Manhattan suburbs. He cut his teeth as a federal prosecutor in New York and the Washington area.
In 2003, the father-of-five became deputy attorney general.
The following year, he faced one of his toughest showdowns, confirming his reputation for being independent and unafraid.
Comey had become acting attorney general due to the illness of his boss John Ashcroft.
At Ashcroft's bedside, the presidential counsel to George W. Bush, Alberto Gonzales, was trying to persuade him to reauthorize a controversial warrantless eavesdropping program.
Comey - who was against extending the program - later revealed the incident to senators, unleashing a political firestorm.
