Asher's first appearance as a child actress was as Nina in the 1952 film Mandy. Other film appearances were the 1955 science fiction film The Quatermass Xperiment, and, co-starring with Kenneth More and Susannah York, in the 1961 UK film The Greengage Summer, which was subsequently released in the United States under the title Loss of Innocence. She also appeared as her distant relative Lady Jane Grey in the 1962 film and Disney TV programme, The Prince and the Pauper. British TV appearances included three episodes (1956–1958) of the British TV series, The Adventures of Robin Hood (working alongside her brother Peter), and as a panellist on the BBC's Juke Box Jury.
McCartney stayed in the Asher family home at 57 Wimpole Street from 1964-66 and wrote several Beatles songs there. He wrote in a room usually used for music lessons. The Asher house was also a place of intellectual stimulation for McCartney. He enjoyed the rarefied atmosphere of upper-middle class conversation and company that the house afforded, and to which he aspired. According to Cynthia Lennon, McCartney was "as proud as a peacock" to have Jane as a girlfriend, and saw her as "a great prize." Marianne Faithfull remembered McCartney and Asher "never getting on very well," and described one evening at Cavendish Avenue when McCartney wanted a window to be open and Asher wanted it shut. McCartney would repeatedly get up and open the window and then Asher would get up and close it, although neither of them made any comment about it during the whole evening.
McCartney did not stop having one-night stands with other women during his time with Asher, because he felt that since they were not married, it was allowed. On 25 December 1967, McCartney and Asher announced their engagement, and she accompanied McCartney to India in February and March 1968. Asher broke off the engagement in early 1968, after coming back from Bristol to find Paul in bed with another woman, Francie Schwartz. They attempted to mend the relationship, but finally broke it off in July 1968. Asher has consistently refused to publicly discuss McCartney or her time with him, and has maintained her position on the matter to this day. On this basis, she is described by the Beatles' 1968 biographer Hunter Davies as the only major Beatles associate not to have published her recollections.
She guest-starred in an episode of the British television comedy series The Goodies in the episode "Punky Business", as a trend setting newspaper writer, patterned on the punk journalist Caroline Coon alias Caroline Kook. In 1994, she portrayed the Doctor Who companion Susan Foreman in a BBC Radio 4 comedy drama Whatever Happened to Susan Foreman?. Another notable radio appearance was in The Further Adventures of Sherlock Holmes in 2002, in the episode "The Peculiar Persecution of Mr John Vincent Harden". She starred in "The World's Biggest Diamond", by Gregory Motton, at the Royal Court Theatre in 2005. In 2006 Asher starred in the Richard Fell adaptation of the 1960s science fiction series A for Andromeda, which aired on the British digital television station BBC Four. More recently in 2007, she portrayed the widow Sandra in the 2007 Frank Oz film Death at a Funeral. Asher appeared in the BBC medical Drama, Holby City as Lady Byrne. In October 2007, she played Andrea Yates in a story in The Sarah Jane Adventures, in the episode "Whatever Happened to Sarah Jane?" She is currently appearing in the ITV drama series The Palace, filmed in Lithuania; she is set to play Queen Charlotte, the mother of King Richard IV. The Palace broadcasts on ITV1 at 9pm every Monday for eight weeks, beginning on the 14 January 2008.
Now well known as an author, Asher has written three best-selling novels: The Longing, The Question and Losing It. She has also had more than a dozen lifestyle, costuming, and cake decorating books published. Asher runs a company making party cakes and sugarcrafts for special occasions, and still acts on television and in the theatre.
She is a shareholder in Private Eye, President of Arthritis Care and a Distinguished Supporter of the British Humanist Association. She is also President of the National Autistic Society, in which she takes an active role. She was also a speaker at the launch of the National Autistic Society's "Make School Make Sense" campaign alongside Joshua Muggleton (ASD speaker/writer). She is also President of the Parkinson's Disease Society.