Vera Cuningham was born in 1897 at Goffs Oak, Hertfordshire. She attended the Central School of Arts and Crafts, where she studied painting. In 1922, she began exhibiting her work with The London Group, and became a member in 1927. After Cuningham met Matthew Smith, they moved to Paris. The British Museum states that they both exhibited in 1922 at the Société des Artistes Indépendants and at the Amis de Montparnasse.
Vera Cuningham also modelled for Smith and his paintings of her between 1923 and 1926 include 'Vera Cuningham', 'Head and Shoulders', 'Vera Cuningham in a Chair', 'Vera Reclining in a Pink Slip', and 'Vera in a Yellow Dress', all of which are in the Corporation of London Collection. In 1929, she had her first solo exhibition at the Bloomsbury Gallery. In the late 1930's, Cuningham produced several theatre designs. She participated in Colling Galleries Civil Defence Artists' shows during World War II. Exhibitions were held in 1948, 1951, and 1954 by Raymond Creuze, her Paris dealer.
She was living in Hampstead, London, at the time of her death in 3 May 1955. A retrospective of her work was held in 1985 by the Barbican Art Gallery.