Before the 1983 NFL draft, the Houston Oilers said they would draft Dickerson second if they did not make a trade. Dickerson’s family opposed him playing for the Oilers, although Dickerson himself was merely cool about doing so, while, like John Elway Dickerson would have flatly refused to play for the Baltimore Colts had they drafted him. A trade with the Oilers saw the Los Angeles Rams acquire the second pick, which they used to draft Dickerson. Although he considered going to the Los Angeles Express in the United States Football League, Dickerson ultimately decided to play for the Rams. An immediate success, he established rookie records for most rushing attempts (390), most rushing yards gained (1,808) and most touchdowns rushing (18), including another two receiving touchdowns. His efforts earned him All-Pro, Pro Bowl, Player of the Year and Rookie of the Year honors.
In his second season, Dickerson continued his onslaught on the NFL record book becoming a member of the 2,000-yard club. Twelve times in 1984 he gained more than 100 yards rushing, breaking the record of 100-yard games in a season held by O. J. Simpson. His 2,105 total yards rushing beat Simpson's 1973 NFL season record of 2,003 yards (Dickerson having reached 2,007 yards after 15 games), but since the NFL expanded the regular season from 14 to 16 games in 1978, Dickerson had the benefit of playing in two additional games. No one has since rushed for more yards in a single NFL season. Dickerson's 5.6 yards per carry led the Rams to a playoff berth in 1984.Although he rushed for 1,234 yards in 1985 while missing the first two games due to a contract dispute, Dickerson missed the Pro Bowl for the first time in his young NFL career. He did go on to rush for a playoff record 248 yards against the Dallas Cowboys in post-season play.
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 fed-up 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.
On April 26, 1992, Dickerson was traded by the Colts to the Los Angeles Raiders for their fourth- and eighth-round picks in the 1992 draft. There were occasional flashes of greatness—107 yards against the Broncos, 103 against the Chargers, where he recorded his 63rd and 64th career 100-yard games—but those would be his last. Dickerson also scored on a 40-yard touchdown run, reminiscent of his prime, in front of a nationally televised Monday Night audience in a game against Kansas City. That year, he led the team in rushing attempts and yards. However, he suffered from splitting carries with Marcus Allen by having the latter finish the second half.
The following season, Dickerson was traded to the Atlanta Falcons on July 7, 1993, for a sixth-round draft pick. He played in a backup role, making his final national televised appearance during the Monday Night Football game on September 27, 1993, when the Falcons hosted the Pittsburgh Steelers in a losing effort. The Falcons traded Dickerson and third-year cornerback Bruce Pickens to the Green Bay Packers for running back John Stephens on October 13, 1993.
The trade came a week after Dickerson said he had been told that the Falcons were waiving him because Coach Jerry Glanville wanted to use younger players. The next day, Falcons officials said that there had been a misunderstanding and that Dickerson had not been placed on waivers. Dickerson retired as the second leading rusher of all time after failing a physical with the Packers.
On August 29, 2017, Dickerson signed a one-day contract to officially retire as a member of the Los Angeles Rams.
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