At the suggestion of the Edinburgh College of Art's Principal Hubert Wellington, Barns-Graham moved to St Ives, Cornwall, in 1940, near to where a group of modernist artists had settled, at Carbis Bay. This was a pivotal moment in her life. Early on she met Borlase Smart, Alfred Wallis and Bernard Leach, as well as the painter Ben Nicholson and the sculptors Barbara Hepworth, Naum Gabo and Margaret Mellis. Barns-Graham became a member of the Newlyn Society of Artists and the St Ives Society of Artists but was to leave the latter when, in 1949, the St Ives art community suffered an acrimonious split, and she became a founder member of a breakaway group of abstract artists, the Penwith Society of Arts and the Crypt Group that preceded it.  In the same year she married the young author and aspiring poet, and later noted architect, David Lewis; the marriage was annulled in 1960.

Barns-Graham travelled regularly over the next twenty years to Switzerland, Italy, Paris and Spain. With the exception of a short teaching term at Leeds School of Art (1956–1957), where she befriended the artists Terry Frost and Stass Paraskos, and three years in London (1960–1963), she lived and worked in St Ives. From 1960, on inheriting a house outside St Andrews from her aunt Mary Niesh (who had been a support to her throughout her art college years), she split her time between summers in Cornwall and winters in Scotland.

After the war, when St Ives had ceased to be a pivotal centre of modernism, Barns-Graham's work and importance as an artist was sidelined, in part by an art-historical consensus that she had been only as a minor member of the St Ives school.  In old age, however, she received belated recognition. She received honorary doctorates from the University of St Andrews in 1992 and later from the universities of Plymouth in 2000, Exeter in 2001 and Heriot Watt Universities in 2003. In 1999 she was elected an honorary member of the Royal Scottish Academy and the Royal Scottish Watercolourists. She was awarded a CBE in 2001, the same year that saw the publication of the first major monograph on her life and work, written by Lynne Green — W.Barns-Graham : A Studio Life (Lund Humphries). This publication was followed in 2007 by The Prints of Wilhelmina Barns-Graham: a complete catalogue by Ann Gunn (also a Lund Humphries publication). Her work is found in several major public collections in Britain.

Wilhelmina Barns-Graham died in St Andrews on 26 January 2004. She is buried by the western wall of the Eastern Cemetery, not far from the cathedral. She bequeathed her entire estate to The Barns-Graham Charitable Trust, which she had established in 1987.