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In the second preseason game against the Atlanta Falcons on August 15, Williamson left the game with an apparent knee injury. The next day, it was revealed that he tore his ACL, prematurely ending his 2019 season.

On March 18, 2018, the New York Jets signed Williamson to a three-year, $22.50 million contract that includes $16 million guaranteed and a signing bonus of $6 million. Williamson entered training camp slated as a starting inside linebacker. Head coach Todd Bowles named Williamson and Darron Lee the starting inside linebackers to begin the season, alongside outside linebackers Josh Martin and Jordan Jenkins. On September 20, 2018, Williamson collected a season-high 14 combined tackles (eight solo) and made two sacks during a 21–17 loss at the Cleveland Browns in Week 3. In Week 6, Williamson made five solo tackles, a season-high three pass deflections, and intercepted a pass by Andrew Luck in the Jets’ 42–34 win against the Indianapolis Colts. Williamson started in all 16 games in 2018 and recorded a career-high 120 combined tackles (80 solo), six pass deflections, three sacks, and one interception.

On October 22, 2017, Williamson made a career-high tying 14 combined tackles during a 12–9 win at the Cleveland Browns in Week 7. In Week 15, he made six solo tackles and sacked quarterback Jimmy Garoppolo in the Titans' 25–23 loss at the San Francisco 49ers. He finished his fourth season with 92 combined tackles (52 solo), three sacks, and two pass break ups in 16 games and 16 starts. The Tennessee Titans finished second in the AFC South with a 9–7 record and qualified for a Wildcard spot. On January 6, 2018, Williamson started his first career playoff game and recorded one tackle in the 22–21 victory at the Kansas City Chiefs in the AFC Wildcard game. The following week, he recorded nine combined tackles and a pass deflection during the Titans' 35–14 loss at the New England Patriots in the AFC Divisional round. On January 15, 2018, head coach Mike Mularkey and the Tennessee Titans agreed to part ways after being unable to come to terms on future plans. Pro Football Focus gave Williamson an overall grade of 85.6, which ranked tenth among all qualifying linebackers in 2017.

In Week 3, Williamson recorded nine combined tackles, broke up a pass, and intercepted Derek Carr during a 17–10 loss to the Oakland Raiders. The following week, he recorded a season-high 12 combined tackles in the Titans' 27–20 loss at the Houston Texans. On December 11, 2016, Williamson made three combined tackles and forced the first fumble of his career as Tennessee defeated the Denver Broncos 13–10. Williamson finished the 2016 season with a career-high 104 combined tackles (73 solo), two sacks, a pass deflection, and an interception in 16 games and 16 starts. The Tennessee Titans saw significant improvement under their new head coach, going from 3–13 to 9-7 and finishing second in the AFC South, but did not qualify for a playoff berth. Williamson received an overall grade of 76.5 from Pro Football Focus, ranking him 41st among all qualified linebackers in overall grade.

On October 11, 2015, Williamson recorded nine combined tackles and made his first sack of the season on Tyrod Taylor during a 14–13 loss to the Buffalo Bills. He left the game after sustaining a hamstring injury in the fourth quarter and was inactive for the Titans' Week 6 loss to the Miami Dolphins. In Week 7, Williamson recorded five combined tackles, a pass deflection, and made his first career interception off a pass attempt by Matt Ryan in the Titans' 10–7 loss to the Atlanta Falcons. After five consecutive losses head coach Ken Whisenhunt was fired and was replaced with offensive coordinator Mike Mularkey as interim head coach. On November 15, 2015, Williamson collected a season-high 14 combined tackles (seven solo) and was credited with half a sack on Cam Newton during a 27–10 loss to the Carolina Panthers. Williamson celebrated his sack on Cam Newton with teammate David Bass by performing a rendition of the dance from rapper Drake's music video "Hotline Bling". He finished with a total of 102 combined tackles (63 solo), 3.5 sacks, a pass deflection, and an interception in 15 games and 15 starts.

Williamson was selected to play in the 2014 NFLPA Collegiate Bowl.

Williamson was one of 35 collegiate linebackers to attend the NFL Scouting Combine in Indianapolis, Indiana. He completed all of the essential combine drills and finished third among all linebackers in the short shuttle, finished sixth in the 40-yard dash, tied for eighth in the bench press, ninth in the broad jump, and finished 11th in the three-cone drill. On March 14, 2014, Williamson attended Kentucky's pro day, but opted to stand on his combine numbers and only performed positional drills for 20 team representatives and scouts from various NFL teams. During the draft process, he attended a private visit with the Tennessee Titans and Washington Redskins. At the conclusion of the pre-draft process, Williamson was projected to be a fifth or sixth round pick by NFL Draft experts and scouts. He was ranked the eighth best inside linebacker prospect in the draft by Matt Miller of Bleacher Report and NFLDraftScout.com. Miller also named Williamson the biggest sleeper amongst all inside linebackers in the draft.

The Tennessee Titans selected Williamson in the fifth round (151st overall) of the 2014 NFL Draft. He was the 18th linebacker selected in 2014.

May 21, 2014, the Tennessee Titans signed Williamson to a four-year, $2.41 million contract that includes a signing bonus of $194,452.

He made his professional regular season debut in the Tennessee Titans' season-opening 26–10 victory at the Kansas City Chiefs. After being relegated to special teams for the first two weeks, Williams was promoted to the reserve inside linebacker on the defense after starter Zach Brown suffered a torn pectoral in the season-opener. In Week 3, he recorded his first career tackle and made four combined tackles on 13 defensive snaps as the Titans were routed by the Cincinnati Bengals 33–7. On October 5, 2014, Williamson earned his first career start after surpassing Zaviar Gooden on the depth chart. He made seven combined tackles and two pass deflections in a 29–28 loss to the Cleveland Browns in Week 5. In Week 8, Williamson made a season-high ten combined tackles, broke up a pass, and recorded his first career sack on quarterback Ryan Fitzpatrick as the Titans were defeated by the Houston Texans 30–16. On November 17, 2014, Williamson recorded eight combined tackles and sacked Ben Roethlisberger twice during a 27–24 loss against the Pittsburgh Steelers. It marked Williamson's first game with multiple sacks. He finished his rookie season in 2014 with 79 combined tackles (51 solo), four pass deflections, and three sacks in 16 games and 12 starts.

After finishing the 2014 season with a 2–14 record, head coach Ken Whisenhunt hired Dick LeBeau as the assistant head coach and as the co-defensive coordinator with Ray Horton. Williamson remained as the starting inside linebacker entering camp although Zach Brown returned from injury. He was named the starter, along with Zach Brown and outside linebackers Derrick Morgan and Brian Orakpo, to begin the regular season.

Williamson attended the University of Kentucky from 2010 to 2013. In 2010, he played in all 13 games as a true freshman, totaling 10 tackles and one pass break-up. In 2011, he played in all 12 games, recording 49 tackles. In 2012, he started all 12 games, finishing second in the SEC with 135 tackles, which placed seventh nationally in total tackles. He also recorded 4.5 tackles for loss, three sacks, four pass breakups, two forced fumbles, one interception and one fumble recovery. In 2013, in his senior season, he recorded 102 tackles, including four for loss, one sack and two fumble recoveries, and was named a second-team All-SEC selection.

Williamson attended Milan High School in Milan, Tennessee, where he led his team to consecutive 14-1 records as a junior and senior (2008 & 2009), losing only in the state championship finals each year to Alcoa High School. He recorded 125 tackles with one interception and also rushed for 416 yards and seven touchdowns. He collected 119 tackles as a junior, including 21 for loss and set a Tennessee state championship game record with 22 tackles in the title contest. He was named the Region Defensive Player of the Year as a junior and senior.

Avery Milton Williamson (born March 9, 1992) is an American football linebacker for the New York Jets of the National Football League (NFL). He was drafted by the Tennessee Titans in the fifth round of the 2014 NFL Draft. He played college football at Kentucky.