It wasn't one of those classic debate gaffes: Richard Nixon mopping his sweaty brow; Michael Dukakis's robotic response to whether he'd favor the death penalty if someone raped and murdered his wife; or George H.W. Bush checking his watch; or even Al Gore's audible sighs.
With Obama, it was more nuanced. The usually witty and at times-electrifying President who could fire up a crowd better than anyone was confined to a stage he did not want to be on -- and viewers saw that immediately.
He was contemptuous of the whole exercise and surprisingly unprepared to rebut the shape shifting of his opponent, who suddenly morphed from the "severely conservative" governor who skated through the Republican primary to the kind of Massachusetts moderate any swing voter might fall for.
As Donald Trump and Hillary Clinton prepare for their face-off Monday night, Obama's experience four years ago is a searing reminder to the candidates about what's at stake during the first debate. If either of them falter, they won't be on stage together again for nearly two weeks to repair the damage.
Obama hated debates, his former speechwriter Jon Favreau recalled in a recent column for The Ringer
. The President viewed them as phony gladiator matches and "a highly subjective test of style and demeanor over substance and accuracy."
And it showed in his wince-worthy performance that night, his annoyance at having his record challenged, his disengagement, all magnified by the split screen images of the two candidates.
"In the green room, we were on our feet, hooting and hollering; like watching an early Tyson fight," recalled Will Ritter, a Republican strategist who was Romney's 2012 director of advance. "Gov. Romney humbled the sitting president who was too arrogant to prepare."
Former Romney strategist Beth Myers said the side-by-side contrast worked to Romney's advantage.
"Voters saw clearly that Mitt Romney was very ready and able to be President; that he held strong opinions and beliefs and had the confidence in those opinions and beliefs to challenge President Obama," Myers said.
In addition, Romney was trailing and he knew the debate was his shot to close the race. "Mitt went to Denver prepared and ready to rumble," Myers said. "My impression was that President Obama did not -- he was just going through the motions, and voters responded to that. They want their president to earn their vote and on that night President Obama fell short. That didn't happen at the next two debates."
Ritter also noted that up until that point the opinions of many swing voters had been shaped by the attack ads of Obama and his allies, who had relentlessly painted Romney as a heartless corporate raider who had preyed on struggling companies while at Bain Capital.
That night he shattered some of those perceptions: "Republicans got their warrior and independents took a second look," Ritter said.
The polls bore that out. For the first time, Romney surged into the lead over Obama in Gallup and Pew polls.
Obama's former strategist David Axelrod still calls that night a painful memory, in large part because they hadn't anticipated or primed Obama to dissemble Romney's moderate transformation.
"We kind of counseled (Obama) not to engage too much. He took that to the extreme," said Axelrod, now a CNN senior political commentator. Romney "simply shed his tax plan, came in with a much more moderate pitch. Honestly, we didn't do a good job of preparing the president for that."
Favreau noted in his column that the Obama campaign also "underestimated how affable, confident, and charming (Romney) would seem."
The cacophony of Democratic criticism of Obama's performance was intense, and his advisers were blunt in their assessment of his performance. The only way out of the hole he had created was practice. Advisers worked with him on finding the right tone -- sounding less defensive; showing passion about how his policies had translated into helping people; and steering him away from sounding like Professor Obama -- honing his points so they were crisp, clear, concise. And in the end, he won the race convincingly.
What lessons can Clinton learn?
As the Clinton campaign prepares for their matchup with Donald Trump, they clearly trying to avoid any mistakes of that kind.
Holed up in a hotel room near her home in Chappaqua, Clinton has delved into the kind of cramming that she does best.
She has carefully anticipated the factually inaccurate arguments that Trump has used on the trail, preparing to fact check him in real time. She is ready with specifics on what he said during the primaries to guard against any attempt at shape-shifting to a more moderate version of himself.
Trump's debate prep has been serious, but more informal. Advisers close to the real estate magnate said he has been formulating his answers through in-depth talks about the issues with allies like New Jersey Gov. Chris Christie, former New York Mayor Rudy Giuliani and General Michael Flynn.
His advisers expect him to be cool and composed, but ready with fierce counterpunches when Clinton attacks. (His flirtation with inviting Gennifer Flowers to sit in the front row via Twitter may have only been the beginning, one Trump confidant hinted).
Facing an unpredictable Trump, former Obama adviser Dan Pfeiffer said Clinton's main task must be to execute her strategy "and not define success based on whether Trump melts down on stage."
"She wins by seeming calm, collected and presidential -- by not getting sucked into Trump's absurdity," said Pfeiffer, a CNN contributor.
With Romney's shape-shifting in mind, Axelrod noted that Clinton has to be be equally ready to take on both the outrageous Trump and the presidential Trump.
If he uses the stage to try to redefine himself, shed policy positions or express remorse for past statements, Axelrod said, "then her task is going to be to remind people of the voluminous evidence to the contrary."
"She's going to be a tougher opponent than he's ever faced," the former Obama adviser noted. "And he'll be a stranger opponent than she's ever faced."