Dexter was drafted in the fifth round (119th overall) of the 1981 NFL Draft by the Washington Redskins, where he played for nine seasons. During his career with the Redskins, Manley won two Super Bowl Championships titles and was a Pro Bowler in 1986 when he recorded a Redskins single season record of 18.5 sacks.

Dexter then played for the Phoenix Cardinals and Tampa Bay Buccaneers. 

Officially, Dexter had 97.5 quarterback sacks in his career. His total rises to 103.5 when the six sacks he had his rookie year of 1981, when sacks were not yet an official statistic, are included.

Dexter also played two seasons in the Canadian Football League with the Ottawa Rough Riders in 1992 and 1993. 

In 2002, Dexter was named as one of the 70 Greatest Redskins and is a member of the Washington Redskins Ring of Fame. Dexter was considered by many to be one of the best players in NFL History to ever rush the quarterback.