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Stellenbosch Football Club was formed in August 2016 when the Premier Soccer League Executive Committee approved the application from National First Division side, Vasco Da Gama for a name change following the club's relocation from Parow to the Stellenbosch Academy of Sport (SAS) in Stellenbosch.

Sammy Troughton was appointed as head coach and Stellies' first National First Division match was played on 28 August 2016 when the team suffered a 3–1 loss to Mthatha Bucks, with Stanley Muishond scoring the club's first-ever goal during the encounter. The club ended its maiden season in third position on the log standings, clinching the final promotion/relegation playoff spot by one point, but ultimately missed out on promotion during the subsequent mini-league.

Following an unsuccessful attempt to gain promotion, the club parted ways Troughton and replaced him with Steve Barker, who had previously been appointed as an assistant coach mid-way through the season. The team subsequently recorded a split record of 10 wins, 10 draws, and 10 losses to finish eighth in the league, thereby failing to qualify for the playoffs. This ultimately led to a change in ownership in August 2018 when the Stellenbosch Academy of Sport purchased the club to usher in a new era.

The following season, Barker's side secured promotion to the DStv Premiership, the top-flight of South African football, as champions of the National First Division after recording a 0–0 draw against Maccabi FC on the final day of the campaign. Stellenbosch commenced their maiden Premiership campaign with a goalless draw against Chippa United, before going on to end the season in 10th position during a year that was interrupted and affected by the COVID-19 pandemic.

The following season, the club began playing home matches at the Danie Craven Stadium, a traditionally rugby-centric stadium, where it has played the majority of its fixtures since, alternating on occasion with Athlone Stadium in Cape Town. Stellenbosch then finished 14th in the 2020–21 domestic standings, a club-record 4th in the 2021–22 season, thereby qualifying for the first time to compete in the MTN 8 tournament, and 6th in 2022–23 campaign. In December 2023, the club won its first cup competition after being crowned inaugural Carling Knockout champions following a penalty shootout win over TS Galaxy at the Moses Mabhida Stadium in Durban.