Bethel-Thompson graduated from San Francisco's Balboa High School in 2006, where he played football, basketball, and baseball.

[3] In 2004 and 2005, he led his team to the Turkey Bowl, the City's annual championship, held on Thanksgiving Day in Kezar Stadium.

He led the Hornets to a come-from-behind victory over UC Davis in the season finale, throwing a game-winning touchdown pass in the twenty seconds.

After going undrafted in the 2011 NFL Draft, Bethel-Thompson joined the San Jose SaberCats of the Arena Football League.

Bethel-Thompson competed with Jordan Palmer, former Fresno State quarterback Ryan Colburn, and Trevor Harris for the starting job.

He was named to the 53-man active roster just before the start of the 2012 regular season after beating out veteran Sage Rosenfels for the third-string quarterback job.

The signing came in part due to the injury to Matt Cassel, leaving the Vikings with only two healthy quarterbacks on the roster, in Teddy Bridgewater and Christian Ponder.

Players were scouted by numerous NFL and CFL teams during the practices and two games played, and Bethel-Thompson earned an invite to workout at a minicamp for the New York Jets.

[37] He was not offered a contract following the Jets minicamp, and on May 23, 2017, Bethel-Thompson signed with the Toronto Argonauts of the Canadian Football League.

Coming off the injured list after 13 weeks, Bethel-Thompson made his debut on September 23, backing up Argos starter, and fellow Sacramento State alumni Ricky Ray.

[40] Bethel-Thompson entered the game during garbage time, and completed his only pass attempt for 8 yards in the 33–19 victory over the Montreal Alouettes.

After going 2-for-2 for 10 yards during the regular season, Bethel-Thompson was the 2nd string QB[41] as the Argonauts won the 105th Grey Cup over the Calgary Stampeders.

[43] After beating the Lions the following week, Bethel-Thompson went on to start and lose the next six games, resulting in the Argos elimination from playoff contention.

However, Bethel-Thompson was announced the starting quarterback after Franklin was placed on the six-game injured reserve list following the team's Week 3 loss.

[48] After the CFL cancelled the 2020 season due to the COVID-19 pandemic, Bethel-Thompson chose to opt-out of his contract with the Argonauts on August 25, 2020.

[51] Despite signing Nick Arbuckle to a free agent deal, the Argos brought back Bethel-Thompson as quarterback depth right before training camp.

[55][56] On October 26, 2021, Arbuckle was traded to the Edmonton Elks, signaling the Argos' confidence in Bethel-Thompson for the remainder of the season.

[57] Bethel-Thompson and the Argos earned a first round bye but were defeated in the Eastern Division Final by the Hamilton Tiger-Cats.

In the playoffs, he led the Argos past the Montreal Alouettes 34–27, advancing to the Grey Cup final on November 20, 2022.

The Argos earned a one point victory over the Winnipeg Blue Bombers, Bethel-Thompson's second overall Grey Cup and first as a starting quarterback.

[64] In late November 2022, he underwent surgery on the thumb of his throwing hand after suffering an injury in the 109th Grey Cup.

With a record of 7 wins and 3 losses, the Breakers earned a playoff berth, but for the second consecutive season were eliminated by the eventual Champions, the Birmingham Stallions.