As a session guitarist and percussionist, he was crucial to the 60s boom in folk music, but Bruce Langhorne, who has died aged 78, will be best remembered as Bob Dylan’s Mr Tambourine Man. It was Langhorne’s Turkish frame drum, like a giant tambourine with bells attached to its edges, that inspired the “jingle jangle morning” of Dylan’s song on the pivotal Bringing It All Back Home album (1965), showcasing Langhorne’s electric guitar. The record’s mix of electric and acoustic songs cued folk music’s transition into folk rock. “If you had Bruce playing with you, that’s all you would need to do just about anything,” Dylan said.

Langhorne’s often tangential interplay with the veteran studio guitarist Al Gorgoni set the stage for Michael Bloomfield’s guitar on Dylan’s next record, the electric masterpiece Highway 61 Revisited, but he first worked alongside Dylan when they were sidemen on Carolyn Hester’s 1961 debut album, with Dylan on harmonica and Bill Lee (father of film director Spike) on bass. Langhorne at first thought Dylan a derivative “phony”, but after hearing his self-penned songs joined him on guitar; his playing on Corrina, Corrina is a highlight of The Freewheelin’ Bob Dylan (1963). Just as importantly, through Hester, Langhorne met her former husband, Richard Fariña, and his wife, Mimi, Joan Baez’s sister. They hit it off immediately. “Dick is the kind of musician who generates a thread … something other musicians can hang on to and build the whole thing. This is my own conception of how music works,” he said.

The two Richard and Mimi Fariña albums released in 1965 were as groundbreaking as Dylan’s, if less commercially successful. Langhorne’s guitar-playing responses to Mimi’s fingerpicking and Richard’s jarring dulcimer were a creative push toward folk’s new amalgam; in 1965 he also joined the Paul Butterfield Blues Band on stage at the Newport folk festival.

Langhorne’s unusual style, without fingerpicking, was dictated by an accident with a firecracker when he was a 12-year-old violin prodigy, blowing off most of his thumb and two fingers of his right hand. “At least I won’t have to play the violin any more,” he told his distraught mother, Dorothy, on the way to the hospital.

He was born in Tallahassee, Florida, where his father, known as JL, was a professor of English at Florida Agricultural and Mechanical University, a black institution in the still segregated American south. His parents separated when he was four, and he and Dorothy moved to Spanish Harlem, New York, where she supervised public libraries. Bruce attended the prestigious Horace Mann school, but was expelled for alleged gang activity. He later claimed to have stabbed someone and fled to Mexico.

He returned aged 17, playing the guitar, first on the streets of Provincetown, Massachusetts, and New York, where he became an accompanist to Brother John Sellers, who was also the MC at Gerde’s Folk City, the hub of the folk movement in Greenwich Village. Like Django Reinhardt, he had to create a unique style using only three fingers. He formed a sextet, the Folksingers of Washington Square, alongside Sandy Bull, with whom he shared a love for African rhythms and the gospel guitar-playing of Roebuck “Pops” Staples. It was Bull who helped him find that sound by lending him an amplifier, into which he plugged his 1920s Martin guitar with a small electric pickup stuck in its sound hole. He was quickly in demand as an accompanist to acts as varied as the Clancy Brothers and Tommy Makem, Peter, Paul and Mary, Judy Collins and Buffy Sainte-Marie. He played with Alvin Ailey’s African-American dance company, where he met the dancer Georgia Collins; their marriage lasted 18 months. He then toured with the folk singer Odetta; in August 1963 they performed in Washington just before Martin Luther King gave his “I have a dream” speech and can be seen in recordings standing behind King on the stage.

As folk-rock morphed into the singer-songwriter era, Langhorne played on Eric Andersen’s Avalanche (1969), and with singers as varied as Tom Rush, Noel Harrison and the former Blues Project vocalist Tommy Flanders. He branched out, recording with the African jazz trumpeter Hugh Masekela, and, in 1971, composing the music for Peter Fonda’s excellent western The Hired Hand. He played on Dylan’s soundtrack for Pat Garrett and Billy the Kid (1973), and scored Fonda’s Idaho Transfer and Jonathan Demme’s Fighting Mad (1976), which starred Fonda. His understated style was highly influential, especially on film-scoring guitarists such as Ry Cooder. Langhorne’s other credits included Bob Rafelson’s Stay Hungry (1976) and Demme’s Melvin And Howard (1980).

Unsuited, he claimed, to the politics or partying of Hollywood, Langhorne moved to Hawaii and farmed macadamia nuts. He returned to Los Angeles in 1985, ran a studio, composed occasional film scores, and played on records with the Nigerian drummer Babatunda Olatunji and Mickey Hart of the Grateful Dead. After being diagnosed with diabetes and having to change his diet, he created a low-sodium African hot sauce, Brother Bru-Bru’s, which became hugely successful.

Following a stroke in 2006 he had to give up the guitar, but he played the piano on his only solo record, Tambourine Man (2011), on which he also sang with a strong Caribbean flavour. His final score was a beautiful composition for a documentary short, Walden (2012) about Thoreau’s pond. In February this year, Scissor Tail Records released a double-album tribute to Langhorne called The Hired Hands.

He is survived by his wife, Janet Bachelor.

• Bruce Langhorne, guitarist, born 11 May 1938; died 14 April 2017