The Baltimore Ravens were leading the San Francisco 49ers 28-6 when most of the lights in the 73,000-seat building went out with 13:22 left in the third quarter.
Auxiliary power kept the playing field from going totally dark, but escalators stopped working and the concourses were only illuminated by small banks of lights tied in to emergency service.
Philip Allison, a spokesman for Entergy New Orleans, which provides power to the stadium, said power had been flowing into the stadium before the lights failed.
"All of our distribution and transmission feeds going into the Superdome were operating as expected," Allison said.
He said the outage appeared to originate in a failure of equipment maintained by stadium staff. It occurred shortly after Beyonce put on a 12-minute halftime show that featured extravagant lighting and video effects.
On the CBS broadcast, play-by-play announcers Jim Nantz and Phil Simms went silent.
CBS sideline reporter Steve Tasker announced the problem of a "click of the lights" to viewers. Later, the halftime crew anchored by host James Brown returned to fill the time with football analysis. Brown said a power surge caused the outage.
"We lost all power up here at the press box level," Nantz said after power was restored. He and Simms were off the air for most of the 34-minute outage.
The failure occurred shortly after Jacoby Jones returned the opening kickoff of the second half for a 108-yard touchdown, the longest play in Super Bowl history and pushing the Ravens to a commanding lead. But when play resumed, the momentum totally changed.
The Niners scored two straight touchdowns and nearly pulled off a game-winning drive in the closing minutes. They had first down inside the Ravens 10, but Baltimore kept them out of the end zone to preserve a wild 34-31 victory.
The blackout, it turned out, became more of a footnote than a spark to the greatest comeback in Super Bowl history.
Still, it was a moment like no other in the title game.
The public address announcer said the Superdome was experiencing an interruption of electrical service and encouraged fans to stay in their seats. Some fans did the wave to pass the time. Players milled around on the sidelines, some took a seat on the bench, other on the field. A few of the Ravens threw footballs around.
Officials gathered on the field and appeared to be talking to stadium personnel. Finally, the lights came back on throughout the dome and the game resumed.
"Let's go!" referee Jerome Boger said to the teams.
The NFL said stadium officials were investigating the cause, but there was no immediate word of why the power went out.
"We sincerely apologize for the incident," Superdome spokesman Eric Eagan said.
He told The Associated Press that Superdome technical staff were working more than hour after the outage to determine what caused it but still didn't know.
Once the game resumed, CBS said all commercial commitments for the broadcast were being honored. The network sold out its allotment of advertising at $3.8 million per 30-second spot.
"We lost numerous cameras and some audio powered by sources in the Superdome," said Jennifer Sabatelle, vice president of communications for CBS Sports. "We utilized CBS' backup power and at no time did we leave the air."
The outage provided a major glitch to what has largely been viewed as a smooth week for New Orleans, which was hosting its first Super Bowl since 2002 and was eager to show off how the city has rebuilt since Hurricane Katrina.
Mayor Mitch Landrieu called the power outage "an unfortunate moment in what has been an otherwise shining Super Bowl week for the city of New Orleans."
"In the coming days, I expect a full after action report from all parties involved. For us, the Super Bowl isn't over until the last visitor leaves town, so we're focused on continuing to show our visitors a good time," said Landrieu, a Democrat and former lieutenant governor of Louisiana.
Monique Richard, who is from the north shore of Lake Pontchartrain, had tickets in the upper deck.
"My exact words on the way over here were, 'I hope this goes off without a hitch,' because the city just looked so good, they were doing so well, the weather so good everything was kind of falling into place," she said.
New Orleans was once a regular in the Super Bowl rotation and hopes to regain that status. Earlier in the week, the host committee announced it will bid on the 2018 Super Bowl, which would coincide with the 300th anniversary of the city's founding.
The 38-year-old Superdome has undergone $336 million in renovations since Katrina ripped its roof in 2005. Billions have been spent sprucing up downtown, the airport, French Quarter and other areas of the city in the past seven years.
"Everything shut down," said Carl Trinchero, a 49ers fan from Napa, Calif., who was in the Superdome. "No credit cards, vending machines shut down, everything shut down."
Trinchero said it may have affected the momentum of the game but, given that the Ravens survived the 49ers comeback, "it didn't affect the outcome."
Joked Doug Cook, a Ravens fan from New Orleans: "They didn't pay the light bill."
Still, he admitted to a fleeting fear when the lights went out.
"I started thinking it was a terrorist attack. I was a little nervous," he said.
In the French Quarter, fans didn't appear much concerned with the power outage or delay in play.
"If we can blame Beyonce for lip syncing, we can blame her for the power outage," said Gary Cimperman of Slidell, La., with a laugh as he watched the second half of the game from a bar. "Or maybe Sean Payton called in the outage, bounty get part two."
Even out-of-towners seemed to be taking the outage in stride.
"So we had to spend 30 minutes in the dark? That was just more time for fans to refill their drinks," said Amanda Black of Columbus, Miss.