Initially Williams served as the backup for starting quarterback Jay Schroeder, but after Schroeder became injured, Williams stepped in and led the Redskins to an opening-day victory against the Philadelphia Eagles. It would be one of three times in 1987 that Williams subbed for Schroeder and led the team to victory (the other two were 11/15 vs. Detroit and 12/26 at Minnesota). Williams only started two games, 9/20 at Atlanta and 11/23 vs. the Rams. While both starts were losses, Williams remained the starter at the end of the season. When the Skins made the playoffs, Williams, with his 94.0 passer rating, remained starter. He led the team to Super Bowl XXII in which they routed the Denver Broncos, becoming the first black quarterback to play in a Super Bowl, and as of Super Bowl XLII, the only black quarterback to win one. On Media Day, Williams was reportedly asked one of the most famous questions in Media Day history: "How long have you been a black quarterback?" Although the question has become legendary, the story is seemingly an urban legend, sprung up from a misunderstanding of some of the questions Williams was asked.

Facing legendary Denver Broncos quarterback John Elway, Williams engineered a 42-10 rout, in which the Redskins set an NFL record by scoring five touchdowns in the second quarter. Williams completed 18 of 29 passes for 340 yards, with four TD passes, and was named Super Bowl MVP.
The Super Bowl was clearly the high point of Williams' NFL career. He suffered from injuries the following season, and was outshined by Mark Rypien, who eventually won the starting job from Williams. Williams would play one final season in 1989, as backup to Rypien, during the latter's first Pro Bowl season.
Williams retired with a 5-9 record as Redskins starter (8-9, counting playoffs) and a 38-42-1 record as a regular season starter (42-45-1, including 7 playoff starts). He had 100 passing touchdowns, and 15 rushing touchdowns, in 88 NFL games.
His throwback jersey remains one of the most popular jerseys sold by the Washington Redskins.
On the day before Super Bowl XXII, Williams had a 6-hour root canal surgery performed (under full anaesthetic) to repair an abscess under a dental bridge. The pain of this condition caused him to having not slept for several days, as reported in the book "Hit and Tell:War Stories of the NFL"(/K.Lynch, Foghorn Press).
Williams became the head football coach at Grambling State University in 1998, succeeding the legendary Eddie Robinson. He led the Tigers to 3 consecutive Southwestern Athletic Conference titles from 2000-2002, before leaving to rejoin the Tampa Bay Buccaneers as a personnel executive. 
Williams currently works for Tampa Bay in the club's personnel department. His son Adrian is an accomplished basketball player, who currently plays for Brown.
At the conclusion of Super Bowl XLII, on the 20th anniversary of being named Super Bowl XXII MVP, Williams carried the Vince Lombardi trophy on to the field for presentation to the winning New York Giants.