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The museum was founded in 1958 on the basis of the State Museum of the Tatarstan Soviet Socialist Republic, which brought together works from the collection of the Kazan local historian and archaeologist of the second half of the 19th century Andrey Likhachev: pictures by Vasily Tropinin, Ivan Aivazovsky, Vasily Perov and Ivan Shishkin. Later, works by Ilya Repin, Alexandre Benois and Boris Kustodiev were added to the collection.

Today, the SMFA collection comprises over 25,000 works, including paintings, graphic works, sculptures and decorative and applied art pieces. Specifically, these include European engravings, Old Russian icon-painting of the 16th century, Russian Avant Garde works from the beginning of the 20th century, and a rich collection of works by the artists of Tatarstan.

The museum moved to its building on Ulitsa Karla Marksa (Karla Marksa Street) in 1967. The building is worthy of attention in its own right as a historic site. At the beginning of the 20th century, the commander of the forces of the Kazan Military District, Alexander Sandetsky, lived here. Born in Vilna (now Vilnius), Sandetsky dedicated 40 years of his life to the army, serving in the Western Siberian Military District, the Caucasus and Transbaikalia. Having come to the Kazan province, he only left it briefly during World War I to command the forces of the Moscow Military District. He then returned to Kazan, where he remained right up until he was shot by the Bolsheviks in 1918. The mansion, with its courtyard, annex, stables and park was built especially for his arrival in 1907 and was financed by the Russian Ministry of War. The house was decorated with Persian carpets, rifles and pistols, and adjutants scurried about the stairs and passageways carrying papers. Following the Revolution, a tuberculosis clinic was set up here. As a result, prior to the museum being moved to the building, in order to entirely remove any remaining mold and dust, the internal finishing of the walls was replaced, with much of the historic decorative plastering being lost in the process.

Since 2007, every year an international festival of improvised music is held in the courtyard, Jazz at the Sandetsky Mansion. The festival was founded by the museum's director, Rozalia Nurgaleyeva, and jazz singer Olga Skepner.

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In the 1990s, the museum's founder, the photographer and designer Rustem Valiakhmetov, was an active collector of the relics of the Soviet era. Visiting him on one occasion, the musician Andrey Makarevich remarked, "This is not just a studio, this is a real museum!" and gave him his jeans. This article of clothing was of special significance in the late-Soviet era – the owner of a pair of jeans, a garment that was in extreme deficit at the time, immediately garnered the respect of "non-formal" youngsters, and a musician appearing in jeans was essentially issuing a challenge to the established cultural hierarchy. Following the "jeans" contribution to the future exhibition, other Russian stars, from Garik Sukachov to Sergey Shnurov, followed suit. As a result, in the winter of 2011, an exhibition titled "Jeans as a Cult" was held at the Museum of Fine Arts. In August of 2011, the museum opened in a building built in the mid-19th century, in a former communal apartment that was once home to 20 people.

The exhibition features all manner of artifacts from the Soviet epoch: homemade guitars, posters, books, newspapers, school accessories, clothing, toys, badges and household implements. This is a huge antiques store in which parents can recall their childhood and youth, and talk about the past with their own children. The collection is regularly being added to, not least because a series of rock stars have been invited to the museum and they always contribute items of real worth. Concerts are sometimes staged on the first floor.

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For many centuries, Islamic culture has been enriching the religious variety and wealth of the Russian state. In Kazan, where several religions have been co-existing over hundreds of years, this is perhaps more strikingly evident than anywhere else. In the Kazan Kremlin, for example, side by side stand the Annunciation Cathedral and the Kul Sharif Mosque. The latter is not only the Republic's main mosque – on its ground floor, since February of 2006, it has housed a museum where you can learn in detail about how Islam developed among the Turkic-Tartar peoples of the Volga and Ural regions, from the declaration of Islam as the state religion of the Bulgar Khanate in 922 right up to the modern era.

A central place in the exhibition is taken by the interactive "self-flipping" Quran which allows visitors to really get to know this sacred artifact. You can also see copies of manuscripts and modern publications of the Quran, and view a three-dimensional installation titled "The Kazan Kremlin in the 15th-21th Centuries." Visitors are told about the five pillars of Islam, shown what the interior of the study of the Tartar enlightener Shigabutdin Marjani looked like, and introduced to Tartar women's struggle for rights.