2017

Charlton was selected by the Dallas Cowboys in the first round (28th overall) of the 2017 NFL Draft. He was the seventh defensive end selected and the second of eleven players drafted from Michigan.^[20]

On May 11, 2017, the Cowboys signed Charlton to a four-year, $10.02 million contract that includes $7.73 million guaranteed and a signing bonus of $5.43 million.^[21] He competed with Benson Mayowa, Charles Tapper, and Damontre Moore throughout training camp for a backup defensive end position. The coaching staff named Charlton the backup left defensive end behind DeMarcus Lawrence, who went on to have a breakout season and tied for second in the league with 14.5 sacks.^[22]

Charlton made his regular season debut in the Dallas Cowboys' season-opener against the New York Giants and finished without any statistic in the 19–3 victory. The following game, he made his first career tackle during the Cowboys' 17–42 loss to the Denver Broncos.^[23] He started the season slow, remaining a backup behind DeMarcus Lawrence and Tyrone Crawford. He recorded his first career sack against the Kansas City Chiefs.^[24] In the twelfth game against the Washington Redskins, he had two tackles, one sack and one forced fumble.^[25] He played sparingly as a backup, appearing in 16 games, while posting 19 tackles (one for loss), one pass defended, one forced fumble, 11 quarterback hurries and three sacks, with two of them coming in the last nine games.^[26]

2018

In 2018, he had to compete for playing time against Tyrone Crawford, Randy Gregory and Dorance Armstrong. He came up with the nickname "Hot Boyz" for the defensive line.^[27] It was also portrayed in the media that he started falling out of favor with the defensive coaching staff.

He started the first seven games at right defensive end opposite of DeMarcus Lawrence and was substituted in passing downs. He had a sack in Week 2 against the Giants.^[28] He suffered a shoulder injury in the eighth game against the Tennessee Titans, that forced him to miss five of the next six contests.^[29] His involvement was limited in the Cowboys' two playoff games, playing only 27 total snaps.^[30]

Charlton registered 27 tackles, four tackles for loss (tied for third on the team), one sack, four quarterback hurries, and one fumble recovery. He appeared in 11 games (seven starts), missing five contests because of a shoulder injury that required offseason surgery, and he also had an ankle surgery.^[31][32][33]

2019

In 2019, he entered training camp with his roster spot in jeopardy, even though Randy Gregory was suspended indefinitely and there were injuries among the defensive ends. The media reported about a meeting he had with defensive coordinator Rod Marinelli in the offseason, about concerns with his development.^[34]

In the preseason, his playing time increased by taking advantage of injuries to defensive ends DeMarcus Lawrence, Tyrone Crawford and Robert Quinn. He had solid performances, with the best one coming in the third game against the Houston Texans, where he registered three tackles, two sacks, two quarterback hurries, one pass defensed, two forced fumbles and one fumble recovery. His big night was dampened by injury, leaving the contest on two occasions because of knee and ankle injuries.^[35]

Charlton was a healthy scratch for the first two games of the season, fueling speculation in the media about his future with the Cowboys. It also didn't help that Charlton showed his displeasure through social media. He tweeted the message "free me" on September 15.^[36]

On September 18, 2019, two weeks into the season, Charlton was released by the team to make room to activate suspended defensive end Quinn, after the team failed to find a trade partner.^[37] His tenure with the Cowboys was one of the shortest for a first-round draft choice in franchise history, that didn't involve a career-ending injury.^[38]