On March 9, 2023, Dukes signed with the Toronto Argonauts of the CFL.[5] During the 2023 CFL season, Dukes acted as a backup for starter Chad Kelly and as a short yardage quarterback sneak specialist, scoring his first CFL rushing touchdown on July 3, 2023, against the BC Lions.[6][7] Dukes saw his first action leading the Argonauts offence on August 4, 2023, taking over for an injured Kelly in a 20–7 loss to the Calgary Stampeders.[8] Dukes dressed in all 18 regular season games, starting in two, where he completed 63 of 96 pass attempts for 760 yards with two touchdown passes and three interceptions.[9] He also had 35 carries for 126 yards and eight touchdowns, primarily in short-yardage situations.[9] He also dressed in the East Final loss to the Montreal Alouettes where he had two carries for two yards and one touchdown on his post-season debut.[9]
On May 7, 2024, Kelly was suspended for at least nine games after an investigation into allegations made against him and the Argonauts by a former strength and conditioning coach.[10] Consequently, Dukes was elevated to the starting role for 2024 that he won during training camp.[11]