Singleton was signed as an undrafted rookie free agent by Seattle on May 8, 2015. He signed a three-year contract worth $1,578,500 and received a $3,500 signing bonus. On September 5, he was released.
Singleton was signed to the Vikings' practice squad on December 22, 2015. He was released on April 13, 2016.
Calgary Stampeders
Singleton was drafted by the Calgary Stampeders with the sixth overall pick in the 2016 CFL Draft. He had acquired a Canadian passport in October 2015, having qualified for dual citizenship because his mother was born in Toronto. Under then-recently implemented CFL rules, Singleton's Canadian citizenship automatically qualified him to be counted as a Canadian "national" player - previously, players who did not play a meaningful part of their amateur football careers in Canada were counted as "international" players even if they were Canadian citizens. Singleton signed with the team on May 17, 2016. He made his CFL debut on June 25, 2016 against the BC Lions.
2016 season
Singleton had an exceptional first season in the CFL and quickly became one of the Stampeders important players on defense. Over the course of the season, he played in all 18 regular season games, and the Stamps two playoff games. He contributed 65 defensive tackles, 9 special teams tackles, and 3 forced fumbles.
2017 season
On November 1, 2017, Singleton was announced the team's nominee for the CFL's most outstanding defensive player, most outstanding Canadian and most outstanding player awards, including sweeping all votes in the defensive and Canadian player categories. His 121 tackles going into week 20 of the CFL season were already the most in Calgary Stampeders history.
2018 season
Singleton's 2018 season matched the previous year in tackles with 123. Although he recorded no sacks, Singleton did add 6 special teams tackles for the Stamps, as well as 2 forced fumbles and was named to his second CFL All-Star team.
Philadelphia Eagles
On January 7, 2019, Singleton signed with the Philadelphia Eagles of the National Football League. Singleton played in all four preseason games for the Eagles, and contributed with 28 defensive tackles and one forced fumble. He was waived during final roster cuts on August 30, 2019, but was re-signed to the team's practice squad the next day. On October 16, 2019, Singleton was promoted to the active roster following the release of linebackerZach Brown.
