In the 1965 season, Stabler and Steve Sloan both played quarterback for the team following Namath's departure to the NFL. With the two splitting time at the position, the Crimson Tide won their second consecutive National Championship. The team defeated the Nebraska Cornhuskers in the Orange Bowl, 39–28.
As a junior in 1966, he took over the quarterback position full-time. He led the team to an undefeated, 11–0 season which ended in 34–7 rout of Nebraska in the Sugar Bowl. Despite the unblemished record, the Tide was snubbed by the polls, finishing in third behind Notre Dame and Michigan State.
Expectations were high in Stabler's senior season, though those expectations would not be completely fulfilled. The offense often struggled, and the defense's performance slipped. During the season, Stabler was kicked off the team for cutting class and partying by Bryant, though was given a second chance. The Tide finished with an 8–2–1 record, including a loss to rivals Tennessee. Though the season was lackluster, Stabler would provide a memorable moment in the Iron Bowl. Trailing 3–0 in a game drenched by rain, Stabler scampered through the mud for a 47–yard, game-winning touchdown which gave the Tide a 7–3 victory over rivals Auburn at Legion Field. The play is commonly referred to as the "Run in the Mud" in Alabama football lore.
Overall in his career, Stabler finished his career at Alabama with a 28–3–2 record as a starter.
After suffering severe knee injuries, Stabler became less a scrambling quarterback and more a classic, drop-back passer, known for deadly-accurate passes and an uncanny ability to lead late, come-from-behind drives. During the peak of his career he had an impressive receiving corps consisting of sprinter Cliff Branch, sure-handed Hall of Fame possession receiver Fred Biletnikoff, and a Hall-of-Fame tight end Dave Casper. The Raider philosophy was to pound teams with their running game and then stretch them with their vertical (long passing) game. Although Stabler's arm was not known for great strength, he was a master of the deep ball to Branch, and deadly accurate on intermediate routes to Biletnikoff and Casper. As a starter in Oakland, Stabler was named AFC player of the year in 1974 and 1976, and was the NFL's passing champion in 1976. In January 1977 he guided the Raiders to their first Super Bowl victory, after a narrow playoff victory over the New England Patriots in which he scored the winning touchdown on a quarterback keeper. In the 1977 AFC Playoffs against the Baltimore Colts he threw a crucial 4th quarter pass to Dave Casper that set up a game tying field goal that sent into overtime in which the Raiders eventually won; the 4th quarter pass was dubbed the Ghost to the Post.
Prior to the 1980 season, after a lengthy contract holdout, Stabler was traded to the Houston Oilers for Dan Pastorini. Stabler left the Raiders as their all-time leader in completions (1,486), passing yards (19,078), and touchdown passes (150). The Oilers in turn saw Stabler as the missing ingredient that could finally get them past the rival Steelers and into the Super Bowl. Pastorini lost the starting job in Oakland to Jim Plunkett after an injury, and Plunkett then led the Raiders over Stabler and the Oilers in the playoffs. Stabler played one more season with Houston, but Oiler coach Bum Phillips liked his grit and brought him with him to New Orleans where he finished his NFL career with a three-year stint with the Saints.
Stabler was a care free soul, in the vein of old pros like Bobby Layne and Joe Namath. He was known to study his playbook by the light of a jukebox and for his affinity for female fans. But, as Hall of Fame guard Gene Upshaw said, "When we were behind in the fourth quarter, with our backs to our end zone, no matter how he had played up to that point, we could look in his eyes and you knew, YOU KNEW, he was going to win it for us. That was an amazing feeling."
Of particular note regarding his career, Stabler was the quickest to win 100 games as a starting quarterback having done so in 150 games. This accomplishment was better than Johnny Unitas previous mark of doing it in 153 games. Since then, only Joe Montana and Tom Brady have reached 100 wins quicker. Stabler is also the only quarterback from the NFL's All-1970's team not in the Pro Football Hall of Fame (the other two being Terry Bradshaw and Roger Staubach). In a recent NFL feature listing the top ten players not in the Hall of Fame, Stabler was listed at number six, partly due to his off-field scandals, which in the 70's were less prevalent, or it could be that he never emulated the same success after he left Oakland, or simply the NFL had a conspiracy against the Oakland Raiders team at the time.