Fonda's stage work in the late 1950s laid the foundation for her film career in the 1960s. She averaged almost two movies a year throughout the decade, starting in 1960 with Tall Story, in which she recreated one of her Broadway roles as a college cheerleader pursuing a basketball star, played by Anthony Perkins. Period of Adjustment and Walk on the Wild Side followed in 1962. In Walk on the Wild Side, Fonda played a prostitute and earned a Golden Globe for Most Promising Newcomer. In 1963, she starred in Sunday in New York. Newsday called her "the loveliest and most gifted of all our new young actresses". However, she also had detractors – in the same year, the Harvard Lampoon named her the "Year's Worst Actress" for The Chapman Report. Her next two pictures, Joy House and Circle of Love (both 1964), were made in France; with the latter, Fonda became one of the first American film stars to appear nude in a foreign movie. She was offered the coveted role of Lara in Doctor Zhivago, but turned it down because she didn't want to go on location for nine months.

Fonda's career breakthrough came with Cat Ballou (1965), in which she played a schoolmarm-turned-outlaw. This comedy Western received five Oscar nominations, with Lee Marvin winning best actor, and was one of the year's top ten films at the box office. It was considered by many to have been the film that brought Fonda to bankable stardom. The following year, she had a starring role in The Chase opposite Robert Redford, in their first film together, with two-time Oscar winner Marlon Brando. The film received some positive reviews, but Fonda's performance was noticed by Variety magazine: "Jane Fonda, as Redford's wife and the mistress of wealthy oilman James Fox, makes the most of the biggest female role." She returned to France to make The Game Is Over (1966), often described as her sexiest film, and appeared in the August 1966 issue of Playboy, in paparazzi shots taken on the set. Fonda immediately sued the magazine for publishing them without her consent. After this came the comedies Any Wednesday (1966), opposite Jason Robards and Dean Jones, and Barefoot in the Park (1967), again co-starring Redford.

In 1968, she played the title role in the science fiction spoof Barbarella, which established her status as a sex symbol. In contrast, the tragedy They Shoot Horses, Don't They? (1969) won her critical acclaim and marked a significant turning point in her career; Variety wrote, "Fonda, as the unremittingly cynical loser, the tough and bruised babe of the Dust Bowl, gives a dramatic performance that gives the film a personal focus and an emotionally gripping power." In addition, renowned film critic Pauline Kael, in her New Yorker review of the film, noted of Fonda: "[She] has been a charming, witty nudie cutie in recent years and now gets a chance at an archetypal character. Fon…

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During the 1960s, Fonda engaged in political activism in support of the Civil Rights Movement, and in opposition to the Vietnam War. Fonda's visits to France brought her into contact with leftist French intellectuals who were opposed to war, an experience that she later characterized as "small-c communism". Along with other celebrities, she supported the Alcatraz Island occupation by Indigenous Americans in 1969, which was intended to call attention to the failures of the government with regard to treaty rights and the movement for greater Indigenous sovereignty.

She supported Huey Newton and the Black Panthers in the early 1970s, stating: "Revolution is an act of love; we are the children of revolution, born to be rebels. It runs in our blood." She called the Black Panthers "our revolutionary vanguard ... we must support them with love, money, propaganda and risk." She has been involved in the feminist movement since the 1970s and dovetails her activism in support of civil rights.

Fonda and Barbra Streisand joined with ten other women in the entertainment industry of Greater Los Angeles to establish the Hollywood Women's Political Committee (HWPC) in 1984. The committee's initial goal was to assist in the presidential campaign of Walter Mondale and his running mate Geraldine Ferraro. The Mondale–Ferraro ticket failed against incumbents Ronald Reagan and George H. W. Bush, but HWPC retrenched itself with a list of New Left political goals, and helped to turn the Senate Democratic in 1986. In 1992, HWPC helped to elect a record-breaking number of women legislators, an achievement called the Year of the Woman. Described by observers as carrying forward the same political goals as Fonda and Streisand, HWPC continued its activism through political setbacks of 1994 and 1996, finally dissolving in 1997. During their run, the HWPC was called "the single most-powerful entertainment group" in politics.
On May 4, 1970, Fonda appeared before an assembly at the University of New Mexico, in Albuquerque, to speak on G.I. rights and issues. The end of her presentation was met with a discomfiting silence until Beat poet Gregory Corso staggered onto the stage, drunk. He challenged Fonda, using a four-letter expletive: why hadn't she addressed the shooting of four students at Kent State by the Ohio National Guard, which had just taken place? In her autobiography, Fonda revisited the incident: "I was shocked by the news and felt like a fool." On the same day, she joined a protest march on the home of university president Ferrel Heady. The protesters called themselves "They Shoot Students, Don't They?" – a reference to Fonda's recently released film, They Shoot Horses, Don't They?, which had just been screened in Albuquerque.

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On April 5, 2005, Random House published Fonda's autobiography My Life So Far. The book describes her life as a series of three acts, each thirty years long, and declares that her third "act" will be her most significant, partly because of her commitment to Christianity, and that it will determine the things for which she will be remembered.

Fonda's autobiography was well received by book critics and noted to be "as beguiling and as maddening as Jane Fonda herself" in its review in The Washington Post, calling her a "beautiful bundle of contradictions". The New York Times called the book "achingly poignant".

In January 2009, Fonda began chronicling her return to Broadway in a blog with posts about topics ranging from her Pilates class to fears and excitement about her new play. She uses Twitter and has a Facebook page. In 2011, Fonda published a new book: Prime Time: Love, health, sex, fitness, friendship, spirit – making the most of all of your life. It offers stories from her own life as well as from the lives of others, giving her perspective on how to better live what she calls "the critical years from 45 and 50, and especially from 60 and beyond". On September 8, 2020, HarperCollins published Fonda's book, What Can I Do?: The Truth About Climate Change and How to Fix It.
Fonda's charitable works have focused on youth and education, adolescent reproductive health, environment, human services, and the arts. Fonda marketed her highly successful line of exercise videos and books in order to fund the Campaign for Economic Democracy, a California lobbying organization she founded with her second husband Tom Hayden in 1978. Fonda has established the Georgia Campaign for Adolescent Power and Potential (GCAPP) in the mid-1990s and the Fonda Family Foundation in the late 1990s. In the mid-2000s, Fonda founded the Jane Fonda Foundation in 2004 with one million dollars of her own money as a charitable corporation with herself as president, chair, director, and secretary; Fonda contributes 10 hours each week on its behalf. In 2017, she began selling merchandise featuring her 1970 arrest mugshot on her website, the proceeds of which benefit GCAPP.