The Vitebsk City Executive Committee voted to create the museum on October 23, 1991, two months after the failed Soviet coup and weeks before the formal dissolution of the USSR. The timing matters. For most of the Soviet period, Chagall was a difficult figure to celebrate in his hometown: a Jewish modernist who had served briefly as commissar for art in Vitebsk in 1918, who had then quarreled with Kazimir Malevich over the direction of the local art school, who had emigrated to Berlin and Paris and become world-famous. He was not the kind of painter Soviet cultural officials wanted to claim, and for decades the city did not. The 1991 decision reversed that. The Marc Chagall Art Center at 2 Putna Street opened in 1992 with exhibition space for graphic works. The total museum area is modest, about 294 square meters across five exposition halls and four exhibition halls, but the holdings have been built carefully.

Chagall was a remarkable printmaker, and the Art Center concentrates on what survives of that work. The collection includes woodcuts, etchings, and aquatints, the long series of illustrations he made between 1923 and 1925 for Nikolai Gogol's Dead Souls, his color lithographs from 1956 and 1960 on biblical themes, and the cycle of color lithographs called The 12 tribes of Israel from 1960. Around these are graphic works by other European avant-garde figures who were Chagall's contemporaries and sometimes friends: Joan Miró, Pablo Picasso, Fernand Léger. A scientific library of more than 3,500 volumes supports research into Chagall and his circle. For a small regional museum, the depth in graphics is real.

The Marc Chagall House-Museum opened five years later, in 1997, at 11 Pokrovskaya Street. This is the wooden house Marc's father built in the early 1900s, where the painter spent his youth and which he describes in My Life. The interior holds household items of Vitebsk's townspeople from the late nineteenth and early twentieth centuries, copies of family documents, and works relating to Chagall and his family. The pleasure of the house is its scale. The rooms are small. The light comes through small windows. The boy who lived here would walk a few blocks in any direction and find the synagogues and the wooden houses and the river that ended up in the paintings.

The harder context is the one the museum building cannot fully contain. Vitebsk before the Second World War was a major center of Jewish life, with a community of roughly 37,000 people. After the German army took the city in July 1941, the Jews were forced into the Vitebsk Ghetto on the right bank of the Western Dvina, and beginning in October the population was murdered in a series of mass shootings near the village of Tulovo. Almost the entire community was killed. Among the dead were neighbors of the Chagall family, congregants of the same synagogues, the people whose faces and rooms had populated his paintings for two decades. Chagall himself, by then in New York with his wife Bella, lost his hometown community while he painted it. The Great Lubavitch Synagogue near the museum, where Chagall and his family had once been congregants, stood derelict for decades; as of 2021 the building was listed as available to investors interested in restoration. The synagogue is still standing. The community it served is not. The museum, in this sense, is not just about a painter. It is one of the few places in Belarus that holds the memory of what Vitebsk was before it was emptied.