She began her career as a child actress in 1964, appearing in East of Sudan, Star!, and two adaptations of The Railway Children: the BBC's 1968 television serial and the 1970 film version.

She relocated to the United States in 1974 to pursue a Hollywood career and subsequently appeared in Logan's Run (1976), Amy (1981), An American Werewolf in London (1981), and Child's Play 2 (1990).

During the same period, Agutter continued appearing in high-profile British films, such as The Eagle Has Landed (1976), Equus (1977)—for which she won a BAFTA Award for Best Actress in a Supporting Role—and The Riddle of the Sands (1979).

She supports several charitable causes, mostly ones related to cystic fibrosis, a condition from which her niece suffers, and for her service to those causes was appointed Officer of the Order of the British Empire (OBE) in the 2012 Birthday Honours.

Agutter then moved into adult roles, beginning with Walkabout (1971), in which she played a teenage schoolgirl who is lost with her younger brother in the Australian outback.

[9] Agutter moved to Hollywood at twenty-one and appeared in a number of films over the next decade, including The Eagle Has Landed (1976), Logan's Run (1976), Equus (1977) (for which she won a BAFTA as Best Supporting Actress), An American Werewolf in London (1981), and an adaptation of the James Herbert novel The Survivor (1981).

Agutter has commented that the innocence of the characters she played in her early films, combined with the costumes and nudity in later adult roles such as Logan's Run, Equus, and An American Werewolf in London, are "perfect fantasy fodder".

In 2012 Agutter resumed her Hollywood career, appearing as a member of the World Security Council in the blockbuster film The Avengers; she reprised her role in Captain America: The Winter Soldier (2014).

[19] At a 1989 arts festival in Bath, Somerset, Agutter met Johan Tham, a Swedish hotelier[20] who was a director of Cliveden Hotel in Buckinghamshire.

[20] Agutter lives in London, but has a keen interest in Cornwall[23] and once owned a second home there on the Trelowarren Estate, in one of the parishes on the Lizard peninsula.

[4][26][27] In August 2014, Agutter was one of 200 public figures who were signatories to a letter to The Guardian expressing their hope that Scotland would vote to remain part of the United Kingdom in September 2014's referendum on that issue.