Oakland became the first team to clinch a playoff spot and now, with a 10-3 record, will set its sights on a first-round bye.
Rich Gannon had 221 yards passing and a touchdown for the Raiders, who had not won consecutive division titles in 18 seasons.
"It feels great," said linebacker William Thomas, who picked off Flutie with six minutes left, helping Oakland to its third straight win. "We had the opportunity to do it earlier and we didn't."
San Diego was driving for the potential tying touchdown when Jeff Graham dropped a pass inside the 10-yard line with 14 seconds left.
The game featured six turnovers, all in the second half. Oakland's tim Brown committed one when he muffed a punt and Jerry Rice had a hand in another when a pass by Gannon deflected off his fingertips.
But Flutie made the most costly error. The Chargers faced a 10-6 deficit, but moved to the Raiders' seven with less than six minutes to play. Flutie then threw a pass directly to linebacker William Thomas.
Flutie had three interceptions, completing 19 of 37 passes for 215 yards as the Chargers (5-9) suffered their seventh straight loss and sixth by seven points or fewer this season.
"Total frustration," Flutie said. "We had some great opportunities. I throw three interceptions and the last one killed us."
"We'll be right there in the game and then we just find a way to lose it instead of finding a way to win it," said San Diego rookie running back LaDainian Tomlinson, who had just 46 yards on 17 carries.
Rice had six catches for 93 yards and a touchdown and Charlie Garner carried 19 times for 68 yards for the Raiders, who clinched their 16th division title.
"We have to concern ourselves with what we are doing right now and try to play the best football the next three games," Gannon said. "We got some tough ones."
The Raiders finish the regular season against Tennessee, Denver and the New York Jets as they chase the best record in the AFC.
"We have a lot to look forward to and we have a lot more football to play," Thomas said.
The Chargers have a lot less to look forward to, thanks to another disheartening setback.
Before Thomas' interception, they drove 55 yards in eight plays, including Flutie's five-yard pass to Curtis Conway on fourth and one from Oakland's 22.
Three plays later, Thomas stepped in front of a pass intended for Conway near the goal line and lateraled to cornerback Charles Woodson, who raced to the Raiders 44.
"Sometimes quarterbacks make mistakes," Thomas said. "It's up to us to capitalize on them. He was throwing the ball pretty well early in the day. He was just trying to make a play."
Flutie nearly made enough plays on San Diego's final possession, but his pass on fourth and nine from Oakland's 23 went through the hands of a wide-open Graham, who dropped several balls on the day.
"Yeah, Jeff has given us an awful lot and made some big plays," Chargers coach Mike Riley said. "Obviously, we could have used a few more plays today. It was one of those days."
The Raiders turned Thomas' interception into a 31-yard field goal by Sebastian Janikowski and a 13-6 lead. They also scored a touchdown following an interception by defensive tackle Darrell Russell on the first possession of the second half.
Oakland started the ensuing drive at its own 12 and went 88 yards on 10 plays as Gannon found a wide-open Jerry Rice from 40 yards for a 10-3 lead. It was the longest reception of the season for the first-year Raider and all-time receiving leader.
"Jerry made a great move on the safety," Gannon said. "We just kind off put one out there and the rest he did all himself."
The teams exchanged field goals during an uneventful first half as each punted on four of five possessions.
There was a scare just before the two-minute warning in the first half, when 70-year-old sideline crew member Carl Robbins had a heart attack. He was resuscitated on the field and taken to a hospital.