She acted opposite him in the John Osborne play The Entertainer on the West End in 1957 and on Broadway in 1958.

She also acted in the films Uncle Vanya (1963), Three Sisters (1970), Avalon (1990), Dennis the Menace (1993), 101 Dalmatians (1996), Jane Eyre (1996), Tea with Mussolini (1999), Bringing Down the House (2003) and Mrs. Palfrey at the Claremont (2005).

In 1956 she joined the English Stage Company at the Royal Court Theatre and was cast as Margery Pinchwife in The Country Wife.

She appeared with George Devine in the Eugène Ionesco play The Chairs, and Shaw's Major Barbara and Saint Joan.

In 1957, Plowright co-starred with Sir Laurence Olivier in the original London production of John Osborne's The Entertainer, taking over the role of Jean Rice from Dorothy Tutin when the play transferred from the Royal Court to the Palace Theatre.

Through her marriage to Olivier, Plowright became closely associated with his work at the National Theatre from 1963 onwards.

In the 1990s, she began to appear more regularly in films, including I Love You to Death (1990), Avalon (1990), Enchanted April (1992) for which she won a Golden Globe Award and an Academy Award nomination, Dennis the Menace (1993) where she played Martha Wilson, The Scarlet Letter (1995), Jane Eyre (1996), 101 Dalmatians (1996) where she played the dog nanny, Dance with Me (1998), and Tea With Mussolini (1999).

She was appointed honorary president of the English Stage Company in March 2009, succeeding John Mortimer who died in January 2009.

[13] Plowright's vision declined steadily during the late 2000s and early 2010s due to macular degeneration.

[17][12] Plowright was appointed a Commander of the Order of the British Empire (CBE) in the 1970 New Year Honours[18] and was promoted to Dame Commander of the Order of the British Empire (DBE) in the 2004 New Year Honours.