Fonda exposed acting inside Omaha, Nebraska, which was his father's home town. He began attending a University of Omaha while still within his mid-teens & joined a Omaha Community Playhouse, where numerous an actor (including his father & Marlon Brando) founded his career. Fonda encountered functiin on Broadway where he achieved notice in Blood, Sweat and Stanley Poole, before going to Hollywood to make films.

Fonda's 1st film was a lightly romance Tammy and the Doctor (1963), which he regretted later: around the September 1970 Playboy interview, Fonda derided it as "Tammy and the Schmuckface."

However Fonda's intensity impressed Robert Rossen, the director of Lilith (1964) who at the start envisioned the Jewish actor in the role of Stephen Evshevsky, a mental patient. Fonda snagged a role when grabbing his boss' glasses from either through his desk & putting the children in and then when to look supplementary "Jewish." He as well played a male lead in the "message" film The Young Lovers (1964), about out-of-wedlock maternity. In the area of 1965, Fonda began to experiment with LSD. Through the Byrds, Fonda met The Beatles at a party at The Beatles' rented home within Benedict Canyon in Beverly Hills. Ringo Starr and John Lennon had ingested LSD. Fondthe repeatedly told Lennon that he experienced near died within a self-inflicted rifle accident as a son, & knew what it was such as to become dead. Lennon encountered this topic unpleasant & replied "Shut up about that stuff." However Lennon immortalized Fonda whilst he repeated this story inside his alliterative psychedelic tune "She Said, She Said," which appeared on The Beatles' Revolver (1966) album.

Fonda's 1st counterculture-oriented film role was the lead character "Heavenly Blues, opposite Nancy Sinatra in the Roger Corman-directed film The Wild Angels (1966). Fonda stepped up from a lesser role to take the place of George Chakiris, who was unable or unwilling to ride the Harley-Davidson motorcycle demanded by the part of a Hells Angels chapter president. This film is still remembered for Fonda's "eulogy" delivered at the fiasco of a fallen Angel's funeral service, which was sampled in the Primal Scream recording "Loaded" (1991). Then Fonda played the male lead character in Corman's 1967 film The Trip, a television commercial director experiencing the ambivalence and turmoil of divorce, while taking LSD for the first time. (Fonda credits Jack Nicholson for the screenplay of The Trip. Nicholson does not appear anywhere in that film's credits, which suggests that Nicholson asked to not be credited because of the outcome of the film, particularly its "message" at the tail end.)

In 1968 Fonda made Easy Rider, the independent cult film for which he is best known. Easy Rider was inspired by the The Wild Angels. In Easy Rider, two long-haired bikers travel from Los Angeles to Florida, through the southwest and southern United States, in contrast to the dominant post-WWII, segregationist culture there, and encounter intolerance and violence. Fonda co-wrote and starred in this film with Dennis Hopper, who directed, and also co-wrote the script with Terry Southern. They filmed their cross-country trip almost entirely on location, spending less than US $500,000.00, and released the film in 1969. The trio was nominated for the Academy Award (TM) for Best Writing, Story and Screenplay Based on Material Not Previously Published or Produced.

Fonda took up sailing in the 1970's and acted in a number of lesser-known and B-movies to fund his long voyages: Dirty Mary, Crazy Larry (1974), Race With The Devil and 92 In the Shade (both 1975), The Cannonball Run (1981) and Nadja (1994).

Fonda received critical recognition for his part in ''Ulee's Gold (1997). Fonda portrayed a stoic north Florida beekeeper who, in spite of his tumultuous family life, imparts a sense of integrity to his wayward son, and protectiveness of his drug-abusing daughter-in-law. His performance resulted in a nomination for an Academy Award (TM) for Best Actor.

In 2000 Fonda co-starred in the film Thomas and the Magic Railroad.

In 2004 he did a character voice-over for the character The Truth in the video game Grand Theft Auto: San Andreas.

Fonda has also directed. In 1971, Fonda directed and acted in his independently-produced Western film, The Hired Hand. He directed but did not appear in Idaho Transfer (1973) and directed and acted in Wanda Nevada'' (1979), in which his father also played a small part.

Fonda's choices of film roles are notable for their extreme contrast in type: from the introverted (albeit amoral and drug-dealing) rebel biker in Easy Rider and the upright war-veteran father in ''Ulee's Gold''.