In the early 1930s she met André Breton in Paris, and later started working with Surrealist automatism techniques in her writing and painting.

Although initially acclaimed, art historians have noted that Colquhoun's reputation suffered during and after World War II when British surrealists such as E. L. T. Mesens pamphleted against her former husband, Toni del Renzio.

[4] In 1929, Colquhoun received the Slade's Summer Composition Prize for her painting Judith Showing the Head of Holofernes, and in 1931 it was exhibited in the Royal Academy.

[8] She established a studio in Paris,[7] where she first encountered Surrealists, including René Magritte, André Breton, Salvador Dalí, Marcel Duchamp, and Man Ray[9] and attended the Académie Colarossi in 1931[9] where she read Peter Neagoe's 1932 essay What is Surrealism?

[7] While in Greece, Colquhoun met and became infatuated with a woman, Andromache "Kyria" Kazou, who was the subject of several drawings and paintings and an unpublished manuscript, Lesbian Shore.

She published work in the London Bulletin in 1938 and 1939,[15] visited André Breton in Paris in 1939,[14] and joined the British Surrealist Group in the same year.

[14] In the 1940s, Colquhoun met and began a relationship with the Russian-born Italian artist and critic Toni del Renzio.

[17] According to Eric Ratcliffe, their studio in Bedford Park, London, became an open house for friends, other artists and like-minded individuals.

The copyright for the works she sold (or gifted) during her lifetime was left to The Samaritans, the Noise Abatement Society, and the Sister Perpetua Wing of St Anthony's Hospital, North Cheam.

[3] Colquhoun began to experiment with automatic techniques in 1939,[28] and used a wide range of materials and methods, such as decalcomania, fumage, frottage and collage.

[30] In 1948 she demonstrated automatic techniques on British television, on a BBC programme called The Eye of the Artist, and in 1951 she published another article, "Children of the Mantic Stain".

[34] Dawn Ades sees Colquhoun's treatment of gender as responding to the masculine and patriarchal themes in the art of other surrealists – for instance, where they drew landscapes as women's bodies.

[15] Several of her works explore themes of castration and male impotence, including Gouffres Amers and The Pine Family, while she portrays female sexuality much more positively, such as in Scylla.

[39] In 1939, she created the work Tepid Waters (Rivières Tièdes) which was displayed at her solo exhibition at the Mayor Gallery the same year.

Three works which stand out during the 1940s are The Pine Family, which deals with dismemberment and castration, A Visitation which shows a flat heart-shape with multi-coloured beams of light and Dreaming Leaps, an homage to Sonia Araquistain, the 24-year-old daughter of the ambassador of the ex-Second Spanish Republic in London who committed suicide by jumping nude from the top of a building.

[41] Along with her visual art, Colquhoun was a prolific writer, producing works including poetry, essays, novels, and travel guides.

[57] Though Colquhoun was a relatively unknown artist by her death in 1988 compared to other women surrealists such as Eileen Agar and Dorothea Tanning, more recently there has been renewed interest in her work from feminist and esoteric viewpoints.

[58] In 2012, the scholar Amy Hale noted that Colquhoun "is becoming recognized as one of the most interesting and prolific esoteric thinkers and artists of the twentieth century".