He was born Robert Burns in San Luis Obispo, California. An early friend of Jerry Garcia, they played together in bluegrass bands (such as the Tub Thumpers) in the early sixties, with Hunter on mandolin and upright bass.

Around 1962, Hunter was an early volunteer test subject (along with Ken Kesey) for psychedelic chemicals at Stanford University's research covertly sponsored by the CIA in their MKULTRA program. [McNally 42] He was paid to take LSD, psilocybin, and mescaline and report on his experiences, which were creatively formative for him: "Sit back picture yourself swooping up a shell of purple with foam crests of crystal drops soft nigh they fall unto the sea of morning creep-very-softly mist...and then sort of cascade tinkley-bell like (must I take you by the hand, every so slowly type) and then conglomerate suddenly into a peal of silver vibrant uncomprehendingly, blood singingly, joyously resoundingbells....By my faith if this be insanity, then for the love of God permit me to remain insane." [McNally 42-43]

The first lyrics he wrote for the Grateful Dead were composed while on LSD, and mailed to the band from Arizona: a suite that would later become "China Cat Sunflower"/"The Eleven" (these were originally performed together for a short time). China Cat Sunflower would later find a partner in I Know You Rider. After battling moderate drug addiction, he abandoned his Joycean/Western vision quest and joined his old friend's band, the Grateful Dead, on the first weekend in September 1967, at the small Rio Nido, California gigs. The association was at first informal, but began on an auspicious note, as that weekend he wrote the first verse of one of his better-known songs, "Dark Star". It is perhaps not a coincidence that some Deadheads argue that the Rio Nido gigs were the first in which the band accessed the full power of their psychedelic improvisation style.

Hunter's relationship with the band grew, until he was officially a non-performing band member. When the band was inducted into the Rock and Roll Hall of Fame in 1994, Hunter was included as a band member, the only non-performer ever so honored. The majority of the Grateful Dead's original songs are Hunter/Garcia collaborations, where Garcia composed the music, and Hunter wrote the lyrics. Garcia once described Hunter as "the band member who doesn't come out on stage with us." Hunter also collaborated as a lyricist with the other voices in the Dead, Bob Weir, Phil Lesh, and Ron "Pigpen" McKernan, although over time Weir, the other principal songwriter besides Garcia, switched to using John Perry Barlow as a lyricist.

Hunter called 1970's "Friend of the Devil" the closest he and Garcia came to writing a classic song} Hunter's most-known line is What a long, strange trip it's been, from that year's "Truckin'". Perhaps the apex of Hunter's lyricism came with two suites written in the mid-1970s, "Help on the Way"/"Slipknot!"/"Franklin's Tower" (1975) and "Terrapin Station" (1977).

In 1974 Hunter released the solo album Tales of the Great Rum Runners featuring himself as a singer songwriter. It was followed the next year by Tiger Rose. Neither attracted a large audience. Another of his solo efforts is the extremely rare recording Jack O' Roses, containing the extended version of "Terrapin Station Suite" (sans the non-Hunter "At A Siding") and a solo rendition of "Friend Of The Devil".

In 1983, Hunter convinced Relix Magazine Founder, Les Kippel, to start a record company. Hunter wanted an American outlet for his new project Jack O'Roses.

Since the dissolution of the Grateful Dead in 1995 Hunter has successfully continued his writing career, working on new songs with Jim Lauderdale, Steve Kimock, David Nelson, and Rob Barraco, among others. He also is seen occasionally playing solo acoustic guitar and performing his classic works, as well as newer songs. In 2004 he opened most of The Dead's summer tour. Hunter co-wrote all but one of the songs on the 2009 Bob Dylan album Together Through Life. Hunter and Dylan collaborated on two songs together on Dylan's Down in the Groove album from 1988 and they sporadically worked together during the 1980s. "He also co-wrote, with Nelson, many of the songs on the 2009 New Riders of the Purple Sage album Where I Come From. Hunter is a former Scientologist.

In 2010 Robert co-wrote Patchwork River with Jim Lauderdale. The Album was released on the Thirty Tigers Label.

Hunter published translations of Rainer Maria Rilke's Duino Elegies and Sonnets to Orpheus and has published several volumes of his own poetry.