Williams is known for running aggressive, attacking 4–3 schemes that put heavy pressure on opposing quarterbacks and for his key role in the New Orleans Saints bounty scandal, also known as "Bountygate".

Williams joined the Buffalo Bills as head coach in 2001 along with new team President and general manager Tom Donahoe.

On January 3, 2006, Williams signed a three-year extension to remain with the Redskins, which made him the highest paid assistant coach in the NFL.

The defense ranked within the top ten in the NFC, and the team finished 9–7, with a loss in the wildcard round to the Seattle Seahawks.

[8] For the remainder of the season, Williams ran an inspired defense which performed, along with the rest of the team, to honor Taylor's memory, highlighted by holding star running back Adrian Peterson of the Minnesota Vikings to 27 yards on December 23, 2007,[9] and allowing a franchise-low one yard rushing to the Dallas Cowboys on December 30, 2007, sealing a playoff seed.

[10] After Joe Gibbs retired, Williams was considered to be the most popular candidate to take over as head coach of the Washington Redskins.

However, on January 26, 2008, Williams was fired, along with offensive coordinator Al Saunders, with Jim Zorn ultimately getting the head coaching job.

[11] On February 6, 2008, Williams became the defensive coordinator of the Jacksonville Jaguars, replacing Mike Smith, who had been hired to coach the Atlanta Falcons.

In fact, Williams was so impressive that Payton offered and took a voluntary $250,000 cut in salary to help facilitate his signing with the team.

[16] A league investigation revealed that Williams began the bounty system soon after he arrived in New Orleans, after Payton charged him to make the Saints' defense "nasty."

[19][20] Former NFL coach and current NBC Sports analyst Tony Dungy said that he was certain Williams operated a similar system with the Oilers/Titans as well.

[28] On April 5, documentary filmmaker Sean Pamphilon released audio of a meeting Williams held with his defense before their 2012 divisional playoff game against the San Francisco 49ers.

[29] On December 12, the Associated Press reported that, according to a transcript of the bounty appeal hearing, Williams had testified that he had wanted to shut down the system after the league began investigating, but was overruled by Saints linebackers coach Joe Vitt.

[32] A little over a month later, on March 21, Williams was suspended indefinitely for his role in the Saints bounty scandal,[33] and was fired on January 2, 2013, without ever working a day for the Rams.

[34] On February 7, 2013, Williams was reinstated by the NFL and officially hired by the Tennessee Titans as a senior assistant defensive coach.

[41] Williams guided the Browns to a 5–3 record, including a credible showing against the Kansas City Chiefs, and was responsible for the emergence of Baker Mayfield as the team's quarterback.

On January 16, 2019, Williams was hired as the defensive coordinator for the New York Jets under new head coach Adam Gase.

The firing came after Williams called a controversial zero blitz on a Hail Mary play in an attempt to sack Derek Carr.

However, Carr found Henry Ruggs open, beating corner Lamar Jackson for a game-winning touchdown with five seconds left, thus dropping the Jets to 0–12.