The largest venue for both organisations is their common home, the Opern- und Schauspielhaus at the Willy-Brandt-Platz in the centre of Frankfurt.

Opened in 1782, the Comoedienhaus (comedy house), with a seating capacity of 1,016,[2] was the first permanent venue of theatre in Frankfurt, for both plays and opera.

[4] Both sections (Sparten) were organised as the Vereinigte Stadttheater (Common city theatres), headed by general manager (Generalintendant) Emil Claar [de].

Based on the ruins of the Schauspielhaus, a new facility was created to provide both plays and operas, and realized in stages completed in 1963.

Beginning in 1959, per the designs of architectural firm Apel & Beckert,[7] the facade was completely replaced, with some elements of the old house partly retained inside.

[9][10] The ceiling of the foyer which is common for play and opera is decorated with a sculpture by Zoltán Kemény, Goldwolken (golden clouds).

[23] In 2004, the organisation was changed to an independent GmbH of the city of Frankfurt, with the artistic directors as chief executive officers, as of 2019 Bernd Loebe and Anselm Weber [de].