Faithfull began her singing career in 1964. Her first gigs as a folk music performer were in coffeehouses and she soon began taking part in London's exploding social scene. In early 1964 she attended a Rolling Stones launch party with artist John Dunbar and met Andrew Loog Oldham, who 'discovered' her. "As Tears Go By", her first single, was written and composed by Jagger, Keith Richards, and Oldham, and became a chart success. (The Rolling Stones recorded their version one year later, which was also successful.) She then released a series of successful singles, including "This Little Bird", "Summer Nights", and "Come and Stay with Me". Faithfull married John Dunbar on 6 May 1965 in Cambridge, with Peter Asher as the best man. The couple lived in a flat at 29 Lennox Gardens in Belgravia, London SW1. On 10 November 1965, she gave birth to their son, Nicholas.

In 1966 she took Nicholas to stay with Brian Jones and Anita Pallenberg in London. During this period, Faithfull started smoking marijuana and became best friends with Pallenberg. She began a much-publicised relationship with Mick Jagger that same year and left her husband to live with him. The couple became a notorious part of the hip Swinging London scene. Her voice is heard on The Beatles' song "Yellow Submarine". She was found wearing only a fur rug by police executing a drug search at Redlands, Keith Richards's house in West Wittering, Sussex. In an interview 27 years later with A.M. Homes for Details, Faithfull discussed her wilder days and admitted that the drug bust fur rug incident had ravaged her personal life: "It destroyed me. To be a male drug addict and to act like that is always enhancing and glamorising. A woman in that situation becomes a slut and a bad mother." It was during this time that Faithfull lost three opportunities to appear in films. "I really thought I had blown my career." In May 1967, Graham Nash, who found Marianne Faithfull "unbelievably attractive," wrote and released the hit song "Carrie Anne" with The Hollies, a track which started out as being about Faithfull. In 1968, Faithfull, by now addicted to cocaine, gave birth to a stillborn daughter (whom she had named Corrina) while returning from Jagger's country house in Ireland.

Faithfull's involvement in Jagger's life was reflected in some of the Rolling Stones' best known songs. "Sympathy for the Devil", featured on the 1968 album Beggars Banquet, was partially inspired by The Master and Margarita, written by Mikhail Bulgakov, a book that Faithfull introduced to Jagger. The song "You Can't Always Get What You Want" on the 1969 album Let It Bleed was supposedly written and composed about Faithfull; the songs "Wild Horses" and "I Got the Blues" on the 1971 album Sticky Fingers were allegedly influenced by Faithfull, and she co-wrote "Sister Morphine". The writing credit for the song w…

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Studio albums
• Marianne Faithfull (1965)
• Come My Way (1965)
• Go Away from My World (1965)
• North Country Maid (1966)
• Faithfull Forever (1966)
• Love in a Mist (1967)
• Dreamin' My Dreams (1976)
• Broken English (1979)
• Dangerous Acquaintances (1981)
• A Child's Adventure (1983)
• Rich Kid Blues (1985)
• Strange Weather (1987)
• A Secret Life (1995)
• The Seven Deadly Sins (1998)
• Vagabond Ways (1999)
• Kissin Time (2002)
• Before the Poison (2004)
• Easy Come, Easy Go (2008)
• Horses and High Heels (2011)
• Give My Love to London (2014)
• Negative Capability (2018)
• She Walks in Beauty (2021)

In addition to her music career, Faithfull had a career as an actress in theatre, television and film. Her first professional theatre appearance was in a 1967 stage adaptation of Chekhov's Three Sisters at the Royal Court Theatre, London, in which she played Irina, co-starring with Glenda Jackson and Avril Elgar. The previous year she had played herself in Jean-Luc Godard's film Made in U.S.A.. Faithfull was also featured in the 1967 film I'll Never Forget What's'isname. In the French television film Anna, she sang Serge Gainsbourg's "Hier ou Demain". In 1968, she starred as a black leather-clad motorcyclist in the film The Girl on a Motorcycle (also known as La Motocyclette and Naked Under Leather). It was thanks to this film, starring Alain Delon, that Faithfull became famous in France. The film was preceded by a widely discussed photograph by Paris Match photographer Patrice Habans capturing her beaming as she conversed with Alain Delon, seated to her left, while her then-partner Mick Jagger sat on her other side . She also played in Kenneth Anger's Lucifer Rising. In London 1969 at the Round House, Faithfull played Ophelia in Hamlet, later filmed as Hamlet.

Faithfull's stage work included Edward Bond's Early Morning at the Royal Court Theatre, London, in which she played a lesbian Florence Nightingale; The Collector at St Martin's Theatre in the West End Mad Dog at Hampstead Theatre; A Patriot for Me by John Osborne, at the Palace Theatre; and the role of Lizzie Curry in N. Richard Nash's The Rainmaker, which toured the UK. Her other film roles during the 1970s included Sophy Kwykwer in Stephen Weeks's Ghost Story (AKA Madhouse Mansion); and Helen Rochefort in Assault on Agathon.

Her television acting in the late 1960s and early 1970s included The Door of Opportunity (1970), adapted from W. Somerset Maugham's story, followed by August Strindberg's The Stronger (1971), and Terrible Jim Fitch (1971) by James Leo Herlihy. In 1991, she played the role of Pirate Jenny in The Threepenny Opera at the Gate Theatre in Dublin. Later she performed Kurt Weill's "The Seven Deadly Sins" with the Vienna Radio Symphony Orchestra, a CD of which was released in 1998.

Faithfull played both God and the Devil. She appeared as God in two guest appearances on the British sitcom Absolutely Fabulous. In 2004 and 2005, she played the Devil in William Burroughs' and Tom Waits' musical The Black Rider, directed by Robert Wilson, which opened at London's Barbican Theatre. In 2001, Faithfull appeared in C.S. Leigh's Far from China. She appeared in Patrice Chéreau's Intimacy (2001), and in 2004, in Jose Hayot's Nord-Plage. She appeared as Empress Maria Theresa in Sofia Coppola's 2006 biopic Marie Antoinette.

Faithfull starred in the film Irina Palm, released at the Berlinale film festival in 2007. She played the central role of Maggie, a 60-year-old widow who becomes a sex worker to pay for medical treatment for her ill grandson. Faithfull was nominated for the European Film Award for Best Actress for her work in the film. She lent her voice to the 2008 film Evil Calls: The Raven, but it was recorded several years earlier when the project was titled Alone in the Dark. She appeared in the 2008 feature documentary by Nik Sheehan on Brion Gysin and the dreamachine, titled FLicKeR.

In 2008, Faithfull toured readings of

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