Ayres worked part-time at the AIA Gallery in Soho from 1951 to 1959 before starting a teaching career. 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 1959, Ayres was asked to teach at Bath Academy of Art, Corsham for six weeks. She remained on the teaching staff until 1965. For much of her time at Corsham she shared a teaching studio with Malcolm Hughes. She was a senior lecturer at Saint Martin's School of Art, London, from 1965 to 1978 and became head of painting at Winchester School of Art in 1978. Ayres left teaching in 1981, and moved to an old rectory on the Llyn Peninsula in north-west Wales to become a full-time painter. Ayres' was awarded the Japan International Art Promotion Association Award in 1963 and in 1975 was awarded a bursary by the Arts Council of Great Britain. In 1982 she was named runner up for the John Moores Painting Prize and was shortlisted for the Turner Prize in 1989. She was appointed Officer of the Order of the British Empire (OBE) in 1986, and in 1991 became a Royal Academician. She later temporarily resigned from the Academy, following the broadcast of a BBC Omnibus television documentary about the preparations for the controversial Sensation exhibition hosted by the Academy in 1997 show-casing the Young British Artists. The documentary, according to Ayres, presented an unfair view of the older members of the Academy. Ayres also objected to the inclusion of Marcus Harvey's portrait of the killer Myra Hindley in the exhibition. She is represented by the Alan Cristea Gallery, London. She was appointed Commander of the Order of the British Empire (CBE) in the 2011 Birthday Honours.