Born in Barnstaple, Devon, England, Eyre was educated at Sherborne School, an independent school for boys in the market town of Sherborne in northwest Dorset in southwest England, followed by Peterhouse at the University of Cambridge.
Eyre became the first president of Rose Bruford College in July 2010. He gives "President's Lectures" at this prestigious drama school; his 2012 talk was entitled "Directing Shakespeare for BBC Television". He lives in Brook Green, West London.
Eyre was Associate Director at the Royal Lyceum Theatre, Edinburgh from 1967 to 1972. He won STV Awards for the Best Production in Scotland in 1969, 1970 and 1971. He was artistic director of Nottingham Playhouse from 1973–78 where he commissioned and directed many new plays, including Trevor Griffiths' Comedians.
Eyre was director of the UK's National Theatre (which gained the now little-used prefix Royal during his time there) between 1987 and 1997. He had previously directed a noted revival of Guys and Dolls for the venue in 1982, with Olivier Award-winner Julia McKenzie and Bob Hoskins. He repeated this production in 1996 with Imelda Staunton and Joanna Riding. His diaries from his time at the National have been published as National Service, winning the 2003 Theatre Book Prize.
Other than Guys and Dolls, his most noted theatre productions include Hamlet (twice), with Jonathan Pryce at the Royal Court in 1980 and Daniel Day-Lewis in 1989; Richard III with Ian McKellen; King Lear with Ian Holm; Tennessee Williams' The Night of the Iguana and Sweet Bird of Youth; Eduardo De Filippo's Napoli Milionaria and Le Grande Magia; Henrik Ibsen's John Gabriel Borkman with Paul Scofield, Vanessa Redgrave and Eileen Atkins; Ibsen's Hedda Gabler with Eve Best; and numerous new plays by David Hare, Tom Stoppard, Trevor Griffiths, Howard Brenton, Alan Bennett, Christopher Hampton and Nicholas Wright.
Eyre has also directed operas. His debut was the 1994 production of La traviata at the Royal Opera House which starred Angela Gheorghiu and was conducted by Sir Georg Solti. This production was televised and has subsequently been released on video and DVD.
He directed the musical Mary Poppins in London and on Broadway. On 14 February 2007, Eyre's production of Nicholas Wright's The Reporter premiered at the Royal National Theatre, London. The play explores the social climate in the years before James Mossman's death as well as the reasons for the death itself.
Eyre directed a new production of Bizet's opera Carmen for the Metropolitan Opera's 2009/10 season, starring Latvian mezzo-soprano Elīna Garanča and Roberto Alagna. He returned to the Met for the 2013/14 season where he created and directed a new production of Jules Massenet's Werther with Jonas Kaufmann and Sophie Koch and returned to create and direct the 2014/15 season opening production, Mozart's The Marriage of Figaro,.
Eyre was planning to direct Jon Robin Baitz's stage adaptation of Hollywood legend Robert Evans' memoirs The Kid Stays in the Picture and its sequel, The Fat Lady Sang, but the project was cancelled by the producer.
His production of Noël Coward's Private Lives starring Kim Cattrall and Paul Gross opened at the Music Box Theatre on Broadway in November 2011 following a run in Toronto. He directed The Dark Earth and The Light Sky for the Almeida Theatre, and The Pajama Game for the Chichester Festival Theatre.
Eyre worked as both a director and one of the producers of BBC's Play for Today between 1978 and 1980. He returned to the BBC in 1988 to direct the Falklands War story Tumbledown (starring Colin Firth), which won him the BAFTA Award for Best Director and the Prix Italia.
Eyre was appointed to the Board of Governors of the BBC in November 1995, and in October 2000 was appointed for a second term of office, though he resigned early (with effect from 31 May 2003) due to theatre and film directing commitments.
For film, he directed The Ploughman's Lunch (written by Ian McEwan) in 1983, which won the Evening Standard Award for Best Film, Iris, a biographical film of writer and philosopher Iris Murdoch (starring Judi Dench, Kate Winslet and Jim Broadbent), and Stage Beauty.
Most recently, he directed Notes on a Scandal, the film adaptation of the Man Booker Prize-nominated novel by Zoë Heller, and in 2008, The Other Man, an adaptation of a short story by Bernhard Schlink, starring Liam Neeson, Antonio Banderas and Laura Linney.
He has been the recipient of numerous directing awards including five Olivier Awards. In 1982 he won the Evening Standard Award for Best Director, for Guys and Dolls, and in 1997 for King Lear and Tom Stoppard's The Invention of Love. In 1997 he won an Olivier Lifetime Achievement Award, and awards from The Directors' Guild of Great Britain, the South Bank Show, the Evening Standard and the Critics' Circle.
He was appointed a Commander of the Order of the British Empire (CBE) in the 1992 New Year Honours, and knighted in the 1997 New Year Honours, receiving the honour on 4 March 1997. He became a Patron of the Alzheimer's Research Trust in 2001. He was made an Officier de l'Ordre des Arts et des Lettres in 1998, and was awarded an honorary Doctorate of Letters by the University of Nottingham on 10 July 2008.