The church was designed by Karl Friedrich Schinkel and was constructed in the period from 1824 to 1830 – almost concurrent to the Altes Museum (Old Museum). Schinkel’s initial plans foresaw the creation of a church in the Neoclassical style, in keeping with his (Altes) museum. However, he bowed to the wishes of Crown Prince Friedrich Wilhelm (IV), who wanted the house of worship beside the palace completed in the 'Old German' (Gothic) style. The building’s proportions reveal how the architect nevertheless remained true to his aim 'to refine the Gothic by the ancient'.

Due to the humble financial resources at his disposal, Schinkel designed a single-nave church. In this, he drew inspiration from English college chapels. The construction material – red brick – may have been deliberately reminiscent of Gothic architecture (and in particular to the neighbouring churches of St. Nikolai and St. Marien) but such a choice of material was nonetheless highly unusual for the time. In fact, the Friedrichswerdersche Kirche was the first prestige project to be completed in brick since the Middle Ages.

Once the church was completed, it was used by German and French congregations. The pulpit, altar, and stained glass windows (some of which are original) are visible remnants of the building’s religious use. Badly damaged in the Second World War, the church was at first only provisionally stabilized. It was only when preparations got under way to celebrate the 200th anniversary of Schinkel’s birth that comprehensive renovation commenced, lasting seven years, from 1979 to 1986.

The church was opened in 1987 to coincide with the 750-year celebrations of the founding of Berlin. The East-German authorities put it to use as an additional venue for the Alte Nationalgalerie. After undergoing renewed restoration from 1997 to 2000, the church houses a permanent display of early 19th-century sculpture.