At the University of Tulsa, he started eight games as a redshirt freshman in 1990 after quarterback T.J. Rubley was injured, starting his first career game at Oklahoma. He finished his college career as the school's second-ranked all-time passer, behind Rubley. During his career, he threw for 5,480 yards and 32 touchdowns on 432-of-860 passing. His 2,871 passing yards as a senior were the most by a Tulsa quarterback in 28 years. As a sophomore, Frerotte also handled punting duties for the team and averaged 35.5 yards per punt.
Frerotte was picked in the seventh round of the draft by the Washington Redskins; earlier in the same draft, the Redskins had selected Heath Shuler with their first-round pick (third overall). However, by the next season Frerotte was the starting quarterback due to Shuler's injuries and struggles adjusting to the professional game. Frerotte would retain the starting job until 1998.
In 1999, he played for the Detroit Lions, where he backed up Charlie Batch. Frerotte wound up starting for the Lions in the playoffs while Batch was out with injuries; the Lions lost in the Wild Card round to the Redskins, Frerotte's former team, 27-13.
He joined the Cincinnati Bengals in 2002, winning the starting job before losing the position after three games to Jon Kitna under the soon-to-be-fired Dick LeBeau. His most notable play with the Bengals came against the Cleveland Browns on September 15: Frerotte, attempting to avoid a sack by Orpheus Roye, threw the ball with his left hand (Frerrotte is right-handed) and was intercepted by Browns defensive lineman Kenard Lang, who returned the ball 71 yards to the Bengals 8-yard line.
Frerotte earned the Miami Dolphins starting job in 2005. He started 15 games, guiding the Dolphins to a 9–6 record, throwing for 18 touchdowns and 13 interceptions, completing 52% of his passes and finished the season with a 71.9 quarterback rating.
On April 1, 2008 he returned to the Vikings, signing a two-year, 3.75 million dollar deal. He was Tarvaris Jackson's backup for the first two games of the year. On September 17, 2008, he was named the starter for the rest of the 2008 season by head coach Brad Childress. Frerotte led the Vikings to an 8-3 record before suffering a back injury, which reinstated Jackson as the starter.
On November 30, 2008, Frerotte tied the NFL record for the longest pass from scrimmage by throwing a 99-yard touchdown pass to Bernard Berrian against the Chicago Bears.
Frerotte had expressed interest in being the starting quarterback for the Vikings for the 2009 NFL season, but was released on February 27, 2009, after the team traded for quarterback Sage Rosenfels. The Vikings, however, would end up signing Brett Favre to be their eventual starter.
As of December 2010, Frerotte works for GAIMPlan Consulting which helps high school athletes pick a college.
On January 19, 2011, Frerotte announced he would be taking over as head coach at John Burroughs School in the St. Louis area. His teams were runners up in the state championship game in 2011 and 2012.