FC Ingolstadt began in the 2004–05 Bezirksoberliga Oberbayern, finishing seventh in their debut season.[1] In their second season, they narrowly missed promotion by just one point, securing third place behind FC Forstern and SV Schechen.[2] The following season, they improved to finish as runners-up to SV Schechen.[3] In the 2009–10 season, they finished second, tied on points and goal difference with TSV SF Poing, but with fewer goals scored.[4]
In the 2010–11 season, FC Ingolstadt finished top of the league, earning promotion to the Landesliga Süd.[5] They remained undefeated in their new league, securing a place in the Bayernliga.[6] During their first Bayernliga season in 2012–13, the team finished second, just missing another promotion behind 1. FC Nürnberg.[7] In the following season, they were promoted to the Regionalliga Süd, finishing two points ahead of SV Frauenbiburg.[8]
In the 2018–19 season, FC Ingolstadt became champions of the Regionalliga Süd and won the promotion play-offs against Borussia Bocholt, advancing to the 2. Bundesliga.[9]