The Museum of Russian Icons was established thanks to the initiative of entrepreneur and patron Mikhail Abramov and opened in May 2006. Initially, the museum was located in one of the halls of the "Vereyskaya Plaza" business center in western Moscow, while active work was underway to reconstruct the main building of the museum.

The reconstruction of the building, located on Goncharna Street in central Moscow, was completed in 2010. Two apartment buildings, which were previously in a state of disrepair, were reinforced, fully restored, and transformed into a modern museum complex with a unifying glass atrium. The new museum building was solemnly opened on January 25, 2011, with the ceremony led by the Minister of Culture of the Russian Federation, Alexander Avdeev. With the opening of the new building, the museum expanded not only in terms of exhibition halls but also gained spaces for the storage of exhibits, their scientific study, cataloging, restoration, and technical-technological research. This led to the creation of a special restoration workshop and scientific-cataloging departments.

Since its opening, the museum has received wide public and professional recognition. For example, it became the first private Russian collection to join the International Council of Museums under UNESCO.