Kirov’s museum was opened for the visitors on the 6th of November 1938. At that time, the museum was located in the former mansion of the ballet-dancer MathildeKshesinskaia (Gorky str, 1/3, now Kuibyshev str).
The permanent exhibition has been very extensive. In 1938 the «Condensed History of the All-Union Communist PartyBolsheviks» was published - a significant book that defined the Stalinist ideological canon of the modern history of the Soviet Union for decades. In accordance with the chronology of the 12 chapters of this book, Kirov’s life journey was represented in 14 halls of the museum.
Also in the Museum an furniture of his home office and office in the Smolny was recreated, there was a memorial hall (where Kirov's death mask by the sculptor Manizer was exhibited), and a room devoted to the reflection of the image of the Kirov in art.
Created with the purpose of ideological education of folks, Kirov’s Museum was free of admission. Until 1943 the Museum was administered by the Leningrad City Council, then by Leningrad Regional Party Committee. For some time the museum had a branch - a Kirov’s office in Smolny.
The reason for the transfer of the museum from the mansion of Kshesinskaia to Kirov’s memorial apartment (at former Kirov Avenue, now Kamennoostrovsky pr., 26/28) to be found in the general atmosphere of ‘defrosting’ in the mid-1950s. It was a,n effort to demonstrate the struggle with the "cult of personality" of Stalin and his comrades. Therefore, in 1955, the former mansion of M. Kshesinskaia was turned over the museum of the October Revolution, and since 1956 the Museum of Kirov is in the Kirov’s memorial apartment.
Until the mid-1980s.the priority of the Museum was the promotion of managerial style of the Leningrad Bolshevik leader. The structure of the museum is strictly consistent with the official Soviet historiography. The party and government enactions were the mandatory component of an exhibition. In Soviet times the Museum expositions were under political censorship, and City Administration for Literature and Publishing kept a close watch on the Museum’s exhibition.
Since 1991, Kirov’s memorial apartments is a branch the State Museum of History of St. Petersburg. 1990s - early 2000s was time for looking for the new Museum's mission and a new Museum concept. During this time, an interactive exhibition about the Soviet childhood of 1920-1930 «…For a happy childhood» was created; interactive educational game «Take what you are given», dedicated to the food facility in Leningrad of the 1930s .; multimedia exhibition "All Kamennoostrovsky prospect in the box». On the base of the exhibition The Museum created two computer games «…for a happy childhood»and «All Kamennoostrovsky prospect until 1917».
The museum is included in the list of historical and cultural landmarks of the Russian Federation.