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 . In 1996, he was selected as a member of the 50th Anniversary 49er Modern Era All-Time Team.