Although the line from Munich to Ingolstadt was approved by the Kingdom of Bavaria in October 1863, construction was slow at first.

Discussions about the location of a future station had begun in 1860 as the city was a state fortress and played an important military role.

[6] The initial network of lines from Ingolstadt station was completed with the opening of the Ingolstadt–Augsburg railway from Augsburg in 1874.

The idea of a direct rail connection between the refinery and industrial centre of Ingolstadt and the chemical triangle around Burghausen in eastern Bavaria was raised again on 28 October 1985 at the Bundestag Committee on Transport.

However, this largely took the view that the existing rail capacity on the routes between Ingolstadt and Burghausen via Landshut or Munich was sufficient.

[8] As a railway junction, especially in a city with a traditionally great military importance, Ingolstadt station was a strategic target for Allied air raids during the Second World War.

From 1990 to 1995, the western Danube Valley Railway linking Ingolstadt Hauptbahnhof and Weichering were completely realigned.

With the beginning of the summer 1995 timetable (from 28 May 1995), Intercity-Express trains (on the Dortmund–Munich route) stopped at Ingolstadt for the first time in regular service.

At the small timetable change on 12 June 2005, five ICE train pairs from Ingolstadt to Munich was extended to Nuremberg and the Ruhr.

[17] When the Nuremberg–Ingolstadt high-speed railway was fully integrated into the ICE network on 10 December 2006, Ingolstadt received hourly direct services to Berlin and to Hamburg.

Due to an axle counter fault on the signaling block, the dispatcher had to manually intervene and mistakenly directed the through freight train on to the track occupied by Üg 18263.

On 11 April 2008, representatives of the state of Bavaria and Deutsche Bahn signed an agreement for the redevelopment of the station.

Deutsche Bahn intended to finance the reconstruction of the station from the proceeds from the sale of the land.

Then on 9 June 2011, Deutsche Bahn announced in a press release that a new construction company would take up the work on the station on 4 July 2011.

[26] Shortly afterward work began on the installation of temporary bridges for the creation of the new underpass, which was commissioned on 31 August 2012.

[28] Due to the central location of Ingolstadt in the centre of in Bavaria, the station is an important hub in Deutsche Bahn's network.

This results in the following train services: Ingolstadt Hbf is a node for the regular interval timetable, with Regionalbahn (RB) services from Augsburg, Regensburg and Ulm/Donauwörth meeting there on the hour and trains of the München-Nürnberg-Express meeting there every two hours, thus provide timely interchanges in all directions.

In the peak hour many extra services run that do not have synchronised meetings in Ingolstadt, mostly on the Munich–Ingolstadt–Eichstätt route, which has strong commuting traffic.

Its roof construction was awarded the BDA (Bund Deutscher Architekten, Federation of German Architects) prize in the "urban space" category in 2006.

Due to the lack of lifts, physically disabled people still have to use a ground-level crossing at the northern end of the platforms, which can only be used with the accompaniment of the service staff.

At the south end of the yard there is a locomotive depot (Bahnbetriebswerk) operated by DB Schenker Rail.