Until the beginning of the 19th century, the land on which the church now stands belonged to the Lopukhin family, relatives of Empress Evdokia, the first wife of Peter I. The large manor house was severely damaged in the fire of 1812. In 1817, the plot was acquired by the parish of the Evangelical Lutheran Church of the Holy Apostles Peter and Paul, and the house was converted into a temple. The reconstruction was mainly funded by Prussian King Friedrich Wilhelm III. The church was consecrated in 1819. In 1837, the church got its first organ, on which Ferenc Liszt performed six years later, giving a concert that, according to contemporaries, had a strong impact on the audience; some ladies cried, while others sniffed ether.

In the mid-19th century, when the number of parishioners exceeded 6,000, a decision was made to build a new church. The new cathedral in Gothic style, designed by architect A. Meinhardt, was completed by January 1862. To save costs, parts of the old building were used. A year later, a bell, gifted by Kaiser Wilhelm I, was raised to the two-tiered bell tower.

Half a century later, the church had to be expanded again. In 1903, an architectural competition was held, won by the project of the famous architect V. Valkot. However, the new building, in the form of a three-nave basilica with a gable roof, was constructed by academician of architecture V. Kosov, partially using Valkot's design. The construction of the new building in neo-Gothic style began around the old one, and only after the work was completed was the old church dismantled.

The church hall was renowned for its excellent acoustics. In 1913, Rachmaninoff's "The Bells" was performed here for the first time, and five years later, Mozart's Requiem was performed with the participation of A. Nezhdanova.

In 1918, the "Peter-Paul Church" received the status of the Cathedral of Russia, and later the Soviet Union. However, the church was soon closed. The building was converted into the "Arctica" cinema, and after the war, it housed the "Diafilm" studio. The premises were re-planned, the interiors were destroyed, and the organ was lost. Before the World Festival of Youth and Students in 1957, the spire of the cathedral was completely dismantled.

In the 1990s, the church was returned to the believers, and restoration work was carried out. In 2010, the spire was restored. Today, the church houses a 19th-century organ, previously belonging to the Lutheran Church of St. Michael on Voznesenskaya (now Radio) Street, which was destroyed in 1928. Concerts of organ music are regularly held here.

The church ensemble also includes a chapel built in the 1890s in the southern part of the churchyard, designed by F. Shekhtel.