Ayres was born in Barnes in south-west London. She studied at the Camberwell School of Art where figurative art was promted, which Ayres hated. She left in 1950 and began to paint abstracts, with her first solo exhibition coming in the mid-1950s. Ayres held a number of teaching posts through the 1960s and 1970s, becoming friends with painters such as Howard Hodgkin, Robyn Denny and Roger Hilton. In 1981 she moved to north Wales, and later to Cornwall.
Ayres' early works are typically made with thin vinyl paint in a limited number of colours arranged in relatively simple forms, but later works in oil paint are more exuberant and very colourful, with a thick impasto being used. The titles of her paintings, such as Anthony and Cleopatra (1982) and A Midsummer Night (1990), are usually given after the painting is completed and do not directly describe the content of the painting, but rather are intended to resonate with the general mood of the work.
Ayres was made an OBE in 1986, and in 1991 became a Royal Acedemician. She later resigned from the Academy, in part because of the controversial Sensation exhibition hosted by the Academy in 1997, show-casing the so-called Young British Artists.
Ayres was shortlisted for the Turner Prize in 1989. She married, and then dovirced, the painter Henry Munday. They had two sons.