ESV Ingolstadt joined the Regionalliga Süd (II) in 1963 when the Bundesliga – Germany's professional football league – was formed.

Bundesliga Süd from 1979 to 1981, the club began a descent through tier III to Landesliga Bayern-Süd (IV), last playing in 1993–94.

The sports club itself carried on until it went bankrupt in the summer of 2004 and those football players there were left to join FC Ingolstadt 04.

ESV continues to operate today offering a number of other sports activities while acknowledging FC 04 on its website.

After World War II occupying Allied authorities ordered the dissolution of all organizations in Germany, including sporting associations.

Newly formed FC Ingolstadt began play in the Oberliga Bayern (IV) and managed to finish second in their first season In 2004–05.

Ingolstadt won its debut second division match, but the following months proved less successful for the club and by the mid-winter break they had dropped to 12th place.

Ingolstadt won both legs of the two match play-off and returned to the second division alongside the top two third-tier teams which advanced automatically by virtue of their finishes.

However, after just nine match days and the seventh defeat - Ingolstadt was bottom of the table - the club parted company with Kurz on 30 September.

The professional team set a record on 19 September 2015: With a 1:0 win at Werder Bremen and the preceding victories on 15 August 2015 at 1.

Despite an improved performance in the second half of the season, the team was unable to avoid relegation on match day 33 after a draw at SC Freiburg.

His successor was former professional footballer Stefan Leitl, who had already spent the last six years of his playing career in the service of FC Ingolstadt 04.

After working their way up to fourth place and coming within a few points of the top three, the Schanzers slipped back into mid-table at the end of the season.

After victories against TSV 1860 München and SpVgg Greuther Fürth, the team reached the round of 16 in the DFB Cup for the second time in the club's history, but was eliminated against the outsiders SC Paderborn from the 3rd football league.

After a clear 6:0 defeat at VfL Bochum and a 0:1 at home against FC St. Pauli, coach Leitl was dismissed on 23 September 2018.

Despite the change of coach, the club was unable to turn its fortunes around and also parted ways with sporting director Angelo Vier on 23 October.

Under Oral, the team won five of their last seven league games and moved up to 16th place in the table, which entitled them to take part in the relegation play-off against SV Wehen Wiesbaden.

The team underwent a major shake-up for the 2019/20 season and the contracts of long-serving players such as Marvin Matip and Almog Cohen were not extended or were cancelled.

Luxembourg's Jeff Saibene and his assistant Carsten Rump, a coaching duo who had already trained together at Arminia Bielefeld, joined the Schanzers.

In the second half of the season, which was temporarily interrupted by the COVID-19 pandemic and subsequently played to a close without spectators, they slipped back into mid-table and brought Tomas Oral to the Danube for his third spell in charge.

Under him, the Schanzers were able to get back into the promotion race and reached fourth place with a 2-0 win at TSV 1860 München on the final matchday, which entitled them to relegation to the 2nd Bundesliga against 1.

FC Ingolstadt again reached the promotion relegation play-offs in the following season 2020/21, winning 3-0 in the first match against second-bottom VfL Osnabrück.

After eight games without a win in the league and a DFB Cup exit against Borussia Dortmund, Schubert was dismissed on 8 December 2021.

Of 11 games after the winter break, FC Ingolstadt lost nine (including a 4-1 defeat to Wehen Wiesbaden), drew one and won one, before slipping to 12th place in the table.

As a result, the club parted ways with Rüdiger Rehm after matchday 20 and replaced him with Italian Guerino Capretti, who had coached Ingolstadt's fellow relegated team Dynamo Dresden until spring 2022.

At the beginning of May 2024, the club parted ways with Köllner during the 2023/24 season and replaced him with Sabrina Wittmann, who had previously coached the U19 team.

FC Ingolstadt managed to win the Bavarian State Cup for the first time in the club's history with its head coach Sabrina Wittmann by beating Würzburger Kickers 2:1 in the final.

The Südtribüne Ingolstadt is divided into blocks U and V. When fans of Schanzer midfielder Almog Cohen displayed the flag of his home country Israel in the stadium on April 26, 2015 in support of him at the away match against 1.

FC Union Berlin, the police commander in charge ordered the flag to be rolled up to avert danger.

The rulers and governors of the city on the Danube have always appreciated and protected its strategic location at the river crossing and on important trade routes.