Eric Allan Dolphy Jr. was born June 20, 1928, in Los Angeles, California, to Sadie and Eric Dolphy Sr., immigrants from Panama. He began private lessons on clarinet and saxophone at age six and added oboe in junior high school, attended Susan Miller Dorsey High School, and won a two-year scholarship to the University of Southern California's music school before enrolling at Los Angeles City College. By 1948 and 1949 he was recording with trumpeter Roy Porter's big band, the 17 Beboppers, doubling on baritone and alto saxophone, flute, and soprano clarinet. Drafted into the U.S. Army in 1950, he served at Fort Lewis, Washington, and attended the Navy School of Music starting in 1952; discharged in 1953, he returned to Los Angeles and worked through the decade with reedman Buddy Collette, pianist Eddie Beal, trumpeter Clifford Brown, and bandleader Gerald Wilson.

Dolphy's breakthrough came in 1958, when he joined drummer Chico Hamilton's quintet, touring nationally and appearing in the concert film Jazz on a Summer's Day, shot at the 1958 Newport Jazz Festival. He left Hamilton's band in 1959 and moved to New York, where bassist and composer Charles Mingus, who had known him from the Los Angeles scene, brought him into his Jazz Workshop in 1960. Dolphy appeared that October on the sessions later issued as Charles Mingus Presents Charles Mingus and Mingus (Candid), his first recorded showcase alongside Mingus's most volatile writing.

Between April and December 1960, Dolphy cut his first three albums as a leader for Prestige's New Jazz subsidiary: Outward Bound (recorded April 1, 1960), with trumpeter Freddie Hubbard, pianist Jaki Byard, bassist George Tucker, and drummer Roy Haynes; Out There (recorded August 15, 1960), an unusual quartet built around Ron Carter's cello; and Far Cry (recorded December 21, 1960), which introduced his partnership with 22-year-old trumpeter Booker Little, again with Byard and Carter. That same December he also recorded as a sideman on two Third Stream-adjacent Atlantic dates: Ornette Coleman's Free Jazz: A Collective Improvisation, playing bass clarinet in Coleman's double quartet, and composer Gunther Schuller and pianist John Lewis's Jazz Abstractions, which paired him with guitarist Jim Hall on Hall's "Piece for Guitar and Orchestra." In early 1961 Dolphy joined John Coltrane's band, appearing on the Africa/Brass sessions (May 23 and June 7, 1961, Impulse!) and the Village Vanguard residency that November; Down Beat writer John Tynan branded their exploratory duets "anti-jazz," a charge Coltrane later rejected, crediting Dolphy with a "broadening effect" on his own playing. Dolphy also appeared, billed under the pseudonym "George Lane" to sidestep his exclusive Prestige contract, on Coltrane's Atlantic session Olé Coltrane (May 1961).

In July 1961, Dolphy and Little co-led a two-week engagement at the Five Spot in Greenwich Village; the surviving tape, from July 16, the residency's final night, produced three volumes released between 1961 and 1965 (At the Five Spot, Volume 1 and Volume 2, and the posthumous Memorial Album), with pianist Mal Waldron, bassist Richard Davis, and drummer Ed Blackwell. Little died of kidney failure that October 5, at age 23. Weeks earlier, in September 1961, Dolphy had toured Scandinavia, recording in Copenhagen with a Danish rhythm section (pianist Bent Axen, bassist Erik Moseholm, drummer Jorn Elniff) and in Stockholm with trumpeter Idrees Sulieman, material later issued across several "In Europe" volumes. On March 10, 1963, he taped a broadcast concert at the University of Illinois with a 22-year-old Herbie Hancock on piano, bassist Eddie Khan, and drummer J.C. Moses; shelved for 36 years, it surfaced in 1999 as The Illinois Concert. That July 1 and 3, he recorded an ambitious two-session date in New York with trumpeter Woody Shaw, multi-reedists Prince Lasha and Sonny Simmons, saxophonist Clifford Jordan, bassoonist Garvin Bushell, vibraphonist Bobby Hutcherson, and a rotating rhythm section, issued in pieces as Conversations (1963) and, after his death, Iron Man (1968).

Dolphy's final American studio album, Out to Lunch! (recorded February 25, 1964, for Blue Note), paired his alto saxophone, bass clarinet, and flute with Freddie Hubbard's trumpet, Bobby Hutcherson's vibraphone, Richard Davis's bass, and 18-year-old Tony Williams's drums on five originals built from angular, asymmetrical structures; it is now widely regarded as his masterpiece. That spring he rejoined Mingus for a European tour with pianist Jaki Byard, tenor saxophonist Clifford Jordan, trumpeter Johnny Coles, and drummer Dannie Richmond, documented on the February 4, 1964 Town Hall Concert and a run of European concert tapes. Before a concert in Oslo, Dolphy told Mingus he intended to leave the band and stay in Europe, disillusioned with the American reception of his music and planning to settle in Paris with his fiancee, dancer Joyce Mordecai; he went on to work with expatriate trumpeter Donald Byrd and saxophonist Nathan Davis. On June 2, 1964, at a VARA radio studio in Hilversum, Netherlands, he recorded what became Last Date with pianist Misha Mengelberg, bassist Jacques Schols, and drummer Han Bennink.

Dolphy fell ill after traveling to West Berlin to perform with vibraphonist Karl Berger's trio; he was hospitalized following his first concert there and passed away on June 29, 1964, five days short of turning 36, after slipping into a diabetic coma that hospital physicians reportedly misread as a drug overdose. He was buried at Angelus-Rosedale Cemetery in Los Angeles under the epitaph "He Lives In His Music," and was inducted into Down Beat's Hall of Fame later that year. His influence reached directly into the next generation of reed players, including Anthony Braxton, members of the Art Ensemble of Chicago, and Oliver Lake, and Frank Zappa later paid tribute with "The Eric Dolphy Memorial Barbecue" on Weasels Ripped My Flesh (1970).

Dolphy was one of jazz's rare true multi-instrumentalist innovators, developing an original vocabulary on alto saxophone, bass clarinet, and flute at once rather than treating any of them as a secondary horn; his lines moved in wide, angular intervals that critics and fellow musicians likened to speech patterns and birdsong, a fascination he pursued directly (he was known to study and imitate the calls of finches and other birds). He bridged camps that rarely spoke to each other in 1960 and 1961: a hard-bop-trained sideman who could also hold his own inside Ornette Coleman's free-jazz double quartet and Gunther Schuller's Third Stream chamber writing, and a member of John Coltrane's working band during the stretch when Coltrane's own harmonic and rhythmic freedom expanded most dramatically. Down Beat's 1961 dismissal of the two men's playing as "anti-jazz" marked the low point of his contemporary critical reception; historical judgment reversed it almost entirely. Out to Lunch! is now routinely ranked among Blue Note's most important albums, and Dolphy is recognized as a direct forerunner of the 1960s "New Thing" avant-garde and of later reed stylists including Anthony Braxton and Oliver Lake.