In interviews with NBC News over the last year, Clapper said he was counting down the days to stepping down at the end of Obama's final term in office. He started as a young intelligence officer reporting to his father during the Vietnam War and said that after than 50 years of service it was time to go.
But Clapper's resignation comes as the Trump team has been struggling to put together a cabinet and mulling what's likely to be a change in national security direction once Obama departs.
Clapper, in testimony to the House Select Intelligence Committee on Thursday, said submitting the resignation " felt pretty good."
Clapper's job is to oversee 17 intelligence agencies, including the CIA, FBI, NSA (National Security Agency) and the DEA (Drug Enforcement Agency).
Appointed by Obama and confirmed by the Senate in 2010, Clapper's tenure in office was marked by high profile showdowns over the government's desire to protect its Americans and citizens' civil liberties.
During a tense March 2013 exchange with Democratic Oregon Sen. Ron Wyden over whether the NSA gathers "any type of data at all on millions of Americans," Clapper responded "no" and "not wittingly."
Then in June of that year, The Guardian published documents leaked by whistle blower Edward Snowden, including a top secret court order showing that the NSA had collected phone records from over 120 million subscribers.
Snowden later told Wired magazine that it was Clapper's testimony that prompted him to leak the documents.
In a 2013 interview with Andrea Mitchell, Clapper said he gave the "least untruthful" response to a complicated question. But Wyden, a Democrat, accused Clapper of "not giving a straight answer." And Rep. Justin Amash, a Michigan Republican, flat-out accused Clapper of committing perjury.
Clapper later suffered the indignity of having his own personal accounts hacked by hacker named "Cracka."