FC Ingolstadt 04 was formed in 2004 through a merger of two local rivals, MTV Ingolstadt and ESV Ingolstadt, with the former playing in the Landesliga Bayern-Süd while the later played in the Bezirksoberliga Oberbayern at the time. The first team took MTV's place, having just been promoted to the Bayernliga, while the new reserve side took up ESV's place in the Bezirksoberliga.
The team took two seasons in this league to achieve success, winning promotion to the Landesliga in 2005. In the Landesliga, the side took again two years to move up again, to the Bayernliga, while the first team had begun its climb through the Regionalliga that would eventually culminate in the 2nd Bundesliga. After three seasons in the Bayernliga, the side finished runners-up in the league in 2010–11 and, courtesy to champions FC Ismaning declining promotion, was promoted to the Regionalliga for the following season.
The team became part of the new Regionalliga Bayern in 2012 and has played at this level since, finishing fifth in 2014–15.
With the introduction of the Bezirksoberligas in 1988 as the new fifth tier, below the Landesligas, all leagues below dropped one tier. With the introduction of the Regionalligas in 1994 and the 3. Liga in 2008 as the new third tier, below the 2. Bundesliga, all leagues below dropped one tier. With the establishment of the Regionalliga Bayern as the new fourth tier in Bavaria in 2012 the Bayernliga was split into a northern and a southern division, the number of Landesligas expanded from three to five and the Bezirksoberligas abolished. All leagues from the Bezirksligas onward were elevated one tier.