Ayres was one of the leading abstract painters of her generation. Whilst attending St Paul's Girls' School, London, she taught art at weekends to the children of blitzed Stepney. In 1946, at the age of sixteen, she enrolled at Camberwell School of Arts and Crafts. Ayres exhibited with Young Contemporaries in 1949 and with the London Group in 1951. Her first solo show was at Gallery One, London, in 1956. The following year she was commissioned to create a large-scale mural for South Hampstead High School for Girls. In 1963 her paintings were included in the Whitechapel Art Gallery's ground-breaking exhibition British Painting in the 60s. As well as the vibrant, heavily worked canvases for which she is best known, she was also a dedicated printmaker.

Ayres held a number teaching posts in various art schools, including Bath Academy of Art, Corsham; St Martin's School of Art, London, and Winchester School of Art. She left teaching in 1981, and moved to an old rectory in North Wales to become a full-time painter. In 1987 she relocated to the North Devon-Cornwall border where she remained for the rest of her life. In 1989 she was shortlisted for the Turner Prize, and in 1991 was elected Royal Academician. Ayres was appointed a CBE in 2011.