The original Durlach station was opened in the then independent community of Durlach along with the Heidelberg–Karlsruhe section of the Rhine Valley Railway, opened on 10 April 1843 by the Grand Duchy of Baden State Railway (German: Großherzogliche Badische Staatsbahn).

The Rhine Valley Railway was originally built as a 1,600 mm (5 ft 3 in) line.

The new Durlach station was opened on 9 December 1911 and required a slightly different route for the Mühlacker line to reach it.

The platforms at the Stadtbahn stop were maintained at their original height of 55 cm, as it was not part of the Rhine-Neckar S-Bahn project.

The tram stop is located some 150 metres from the railway station on Durlacher Allee and is called Auer Straße.