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On January 2, 2019, McCoil was signed to the Los Angeles Chargers practice squad.

On October 16, 2019 McCoil was drafted by the St. Louis BattleHawks in the fourth round of the defensive backs phase of the 2020 XFL Draft.

On October 22, 2019 McCoil signed with the Calgary Stampeders near the end of the 2019 regular season. He was cut on November 25, 2019.

On October 9, 2017, McCoil was claimed off waivers by the San Francisco 49ers. He was released on April 30, 2018. He was re-signed by the 49ers on August 17, 2018. He was waived on September 1, 2018. He was re-signed again to the practice squad on September 27, 2018. He was released on October 9, 2018.

On January 12, 2016, he signed with the San Diego Chargers. The Chargers tried him out at linebacker and at safety during their off-season workouts. On September 3, 2016, he was listed on the Chargers' final 53-man roster. McCoil made his first start at safety for the Chargers on September 25, 2016, against the Indianapolis Colts. He played in all 16 games with two starts, recording 25 tackles, five passes defensed and one interception. On October 7, 2017, McCoil was waived by the Chargers.

On February 17, 2014, McCoil was assigned to the Los Angeles Kiss of the Arena Football League (AFL).

On May 31, 2014, he signed with the Edmonton Eskimos of the Canadian Football League. He won the CFL's Most Outstanding Rookie Award in 2014 for recording 67 tackles, four sacks and tying for the league lead with six interceptions. McCoil and the Eskimos had a contract dispute during the 2015 CFL season as he claimed that he was not offered the 1-year contract (with a player option to extend to 2 years), rather he claimed the Eskimos only offered him the minimum 2-year contract. On the field McCoil continued to be a key cog in the Eskimos defense recording 76 defensive tackles, two sacks, three interceptions and a fumble recovery. On December 6, 2015, after winning the 103rd Grey Cup to close the season, the Eskimos announced they had reached a settlement of all outstanding matters with Dexter McCoil, the CFL and the CFLPA. Starting on May 1, 2016, McCoil was free to attempt to sign with an NFL team. In the event that McCoil was unsuccessful in securing an NFL standard player contract for the 2016 NFL season, he entered into an agreement to play for the Eskimos for the 2016 and 2017 CFL seasons.

McCoil went undrafted following the conclusion of the 2013 NFL Draft. McCoil attended the Oakland Raiders rookie minicamp but failed to make the final cut on the preseason 90 man roster.

McCoil was named the Defensive MVP following his performance in the 2011 Bell Helicopter Armed Forces Bowl. He also earned second-team all-Conference USA honors following his Junior season. Prior to his Senior season, he was selected on the Bronko Nagurski Trophy Watch List and also selected on the Jim Thorpe Award Watch List. In his four seasons at Tulsa, he finished with a total of 315 tackles, 18 Interceptions, 43 passes defensed, and one forced fumble.

McCoil attended Lutcher High School in Lutcher, Louisiana, where he helped lead the Bulldogs to the 2008 3A State Championship. He was ranked as the 58th top prospect in the state of Louisiana by Rivals.com. He was named the District MVP following his senior season. He was an honorable mention all-state in his Senior season. McCoil also earned the all-district, all-metro and all-River Parish honors following both his junior and senior seasons of high school.

Dexter McCoil (born September 5, 1991) is an American football safety for the St. Louis BattleHawks of the XFL. He played college football at Tulsa. McCoil has also been a member of the Los Angeles Kiss, Edmonton Eskimos, Los Angeles Chargers, San Francisco 49ers, and Calgary Stampeders.