By the end of the 1920s, more than 100 anti-religious museums had been opened in the Soviet Union. In addition, anti-religious departments appeared in the exhibitions of many local historical museums. In Moscow, the Central Anti-Religious Museum was opened in the Cathedral of the Strastnoi Monastery. At that time, the first museum promoting a comparative and historical approach to the study and presentation of religious artifacts was opened in Petrograd in 1922. The formation of Museum of Comparative Religion was based on the conjunction of the activities of the Petrograd Excursion Institute, the Academy of Sciences, and the Ethnographic department of Petrograd University. In this paper, based on archival materials, we analyze the methodological principles of the formation of the exhibitions at the newly founded museum, along with its themes, structure, and selection of exhibits. The Museum of Comparative Religion had a very short life before it was transformed into the Leningrad anti-religious museum, but its principles were inherited by the Museum of the History of Religion, which was opened in 1932.