In 1990, Carter was drafted in the 1st round by the 49ers, the winner of the previous 2 Super Bowls, with the hopes of taking some of the running game responsibility from Roger Craig as well as serving as the primary kick returner. He led the team in rushing in his rookie season with 460 yards after Craig missed 5 games with injury. He was the second-leading rusher in 1991 behind Keith Henderson, but then fell on the running back depth chart the following year and became almost exclusively a kick returner after that. He was a contributor in this capacity to the 49ers' Super Bowl XXIX team in 1994.
In that offseason, he signed a free agent three-year contract with the Jets worth about $1.7 million. He struggled on his new team, fumbling 7 times (losing 4) in 10 games before being cut on November 8. He was then picked up by the 49ers and resumed his role as their kick returner the next week. He created NFL history that season by becoming the only player ever to record at least one touch and one all purpose yard in 17 regular season games. He did this by playing for the Jets before their bye week and being signed by the 49ers after their bye week.
Carter finished his 7 NFL seasons with 1,042 rushing yards and 5 touchdowns, along with 59 receptions for 652 yards and 2 touchdowns. On special teams, he returned 138 punts for 1,358 yards and 2 touchdowns, while also returning 250 kickoffs for 5,412 yards and 2 touchdowns.
In 2007, Dexter returned to Florida State University as the running backs coach but was not retained after the 2009 season as incoming head coach Jimbo Fisher brought in his own coaches when taking over for Bobby Bowden.