In 1919 Vera Yermolaeva moved to Vitebsk, where she held the post of the rector of the National Art School (1920–1922) after Mark Chagall had left it. Under the influence of Kazimir Malevich she turned to the non-figurative abstract art. She was the stage director of the classical Suprematist play production Victory over the Sun (1920), and was one of the active members of the UNOVIS avant-garde art group founded and headed by Kazimir Malevich. Vera Yermolaeva created a range of Suprematist monumental and decorative projects to embellish the city during revolutionary celebrations. Later she joined the staff of the Leningrad Institute of Art Culture (Inkhuk, 1923–1926), where she implemented a number of theoretical and experimental works in the colour laboratory. By the late 1920s Vera Yermolaeva followed her teacher back to figurative art in the spirit of metaphysical painting. She also worked as an illustrator for children’s books and magazines. Her best children's books were co-created jointly with the avant-garde poets A. I. Vvedensky (Fishermen, 1929) and Daniil Kharms (Ivan Ivanych Samovar, 1930). In 1934 Vera Yermolaeva created a cycle of color lithographs to Goethe’s satirical poem Reineke Fox (Russian Museum), which allegorically reflected political realities of that time.
 

In 1934 the artist fell victim to Stalinist repressions: she was accused, arrested and sent to Karaganda, where she was shot down in 1937.