1987–1991: Indianapolis Colts
The 1985 season marked the beginning of ongoing contract disputes between Dickerson and the Rams. In 1987, after playing just three games for the Rams during the strike-shortened 1987 season, Dickerson was traded to the Indianapolis Colts in one of the NFL's biggest trades ever at that time. In a three-team deal, the Colts traded linebacker Cornelius Bennett, whom they drafted but were unable to sign to a contract, to the Buffalo Bills for their first-round pick in 1988, first- and second-round picks in 1989, and running back Greg Bell. The Colts in turn traded Bell and the three draft choices from Buffalo plus their own first- and second-round picks in 1988, their second-round pick in 1989, and running back Owen Gill to the Rams for Dickerson. With the picks the Rams took running back Gaston Green, wide receiver Aaron Cox, linebacker Fred Strickland, running back Cleveland Gary, linebacker Frank Stams, and defensive back Darryl Henley. The trade reunited Dickerson with Ron Meyer, who had left SMU after Dickerson's junior season to take the head coaching position in New England and who was hired by the Colts in 1986 following Rod Dowhower's firing.
Although he played in just nine games with the Colts that year, he still managed to gain 1,011 yards to finish the season with 1,288. Also, he spearheaded a late season Colts run that helped the team to their first winning season (and first playoff berth) in 10 years.
In 1988, Dickerson, with 1,659 yards rushing, became the first Colt to lead the league in rushing since Alan Ameche in 1955. This would mark the apogee of Dickerson's career with the Colts (although he would gain 1,311 yards rushing in 1989). Also, 1989 was the year that he passed the 10,000-yard mark, becoming the fastest player ever to do so (91 games), accomplishing the feat faster than greats like Jim Brown (98 games), Barry Sanders (103 games), Emmitt Smith (106 games), and LaDainian Tomlinson (106 games). By 1989, he had set a new NFL record with seven straight seasons of more than 1,000 yards rushing, and led the league for four of those seasons. With the retirement of Tony Dorsett at the end of 1988, he became the leader among active players in career rushing yards, a position he occupied until his own retirement in 1993.
However, injuries, further contract disputes, and suspensions clouded his final two seasons with the Colts. Dickerson, at 29, was the highest-paid running back in the NFL, receiving an annual reported salary of $1.4 million. Following prolonged contract disputes, the Colts placed him on the inactive list before the start of the 1990 season where he stayed for 7 weeks and lost more than $600,000 in salary. In his sixth game back from suspension, he rushed for 143 yards against the Bengals on 22 carries—this effort lifted him past Jim Brown to third place on the NFL career rushing list behind Walter Payton and Tony Dorsett. He was again suspended in November 1991, and amidst injuries and age, managed to run for only 536 yards that season. The Colts finished the year bottoming out with a 1–15 record.
Dickerson has described the trade to Indianapolis as the worst moment of his career, and stated that he disliked his time with the Colts.