Pruett earned his first collegiate coaching job in 1979 as the defensive line coach for his alma mater, Marshall University. In 1981, he became the defensive backs coach and defensive coordinator for the Herd until the end of the 1982 season. Before the start of the 1983 season, Pruett joined the coaching staff of the Wake Forest Demon Deacons as the defensive backs coach. His lifelong friend, Al Groh, was the head coach of the Demon Deacons at the time. He remained the defensive backs coach until 1985, when he took on the role of defensive coordinator. Though Groh stepped down as head coach of the Deacons in 1986, Pruett kept the job of DC until 1990, when he became the defensive backs coach at Ole Miss the next season. Pruett, known for his diverse defensive coverages, gained high respect in the NCAA, and as a result, would coach as a defensive coordinator or head coach for the rest of his coaching career. The following year, the Tulane Green Wave hired him as their defensive coordinator until the end of the 1993 season, when one of his lifelong goals came true.
Pruett, who had aspired to coach at the University of Florida for quite some time, applied and was employed by Steve Spurrier's staff for the 1994 and 1995 seasons as defensive coordinator. In his first season there, his defense held opposing teams to an average of 84.6 rushing yards per game, and kept those same teams to an average of 17.1 points per game. That season, the Gators played the University of Alabama Crimson Tide in the SEC Championship, in which they won, 24–23. They then accepted a bid to play in the Sugar Bowl against their in-state rivals, the Florida State Seminoles, in which they lost, 17–23.
In his second and final season at Florida, Pruett's defensive squad led the team to an undefeated regular season. Also, the UF defense that year was ranked top 25 in the nation in scoring defense, pass efficiency defense, rushing defense, and total defense. In the SEC Championship that year, the Gators took on the Arkansas Razorbacks and came out with an easy win, with the score 34–3. At #2 in the AP Polls, The Gators were given a bid to play in the Fiesta Bowl in Tempe, Arizona against the also undefeated Nebraska Cornhuskers. The game was a rout, with the Cornhuskers coming away with the victory, 62–24. This game came to be known as the "Fiasco Bowl" due to the lopsided score.
While coaching at Florida, the head coaching job at Marshall University became vacant due to Jim Donnan taking the head coaching job at the University of Georgia. Pruett immediately applied for the position, later Marshall President J. Wade Gilley called Pruett and informed him that the job was his.
In 2008, Pruett came out of retirement to become the defensive coordinator for Virginia. After the 2008 season, Pruett retired again.[3]