He was born Herman Poole Blount in Birmingham, Alabama, on May 22, 1914, and named after the touring stage magician Black Herman. His family called him Sonny. He could sight-read and compose by age eleven, absorbed the touring bands of Fletcher Henderson, Duke Ellington, and Fats Waller when they came through town, and taught himself to transcribe entire big-band arrangements from memory. At Birmingham's segregated Industrial High School he studied under John T. "Fess" Whatley, the music teacher who trained a generation of Alabama players. In 1934 his former biology teacher, the singer Ethel Harper, put him to work in her band; when she left for New York he took it over and renamed it the Sonny Blount Orchestra. A scholarship took him to Alabama Agricultural and Mechanical University in 1936, but he left after one year. He later described the reason as a visionary experience in which he was transported to Saturn and instructed to abandon college and speak to the world through music. He recounted that account consistently for the rest of his life and treated Saturn, not Alabama, as his origin.

Drafted in October 1942, Blount declared himself a conscientious objector on religious grounds and because he was supporting his great-aunt Ida. He failed to report to the Civilian Public Service camp assigned to him in Pennsylvania, was arrested in Alabama that December, and spent time in the Walker County jail before his objector status was reaffirmed in February 1943. He was reclassified 4-F in March 1943 on account of a hernia and returned to Birmingham. After his great-aunt's death he joined the Second Great Migration and moved to Chicago in 1945. His recording debut came the following year backing the blues shouter Wynonie Harris on "Dig This Boogie." In August 1946 he began a long engagement at the Club DeLisa as pianist and arranger for Fletcher Henderson, the man whose records he had studied as a boy, and in 1948 he worked briefly in a trio with Coleman Hawkins and the violinist Stuff Smith. Away from the bandstand he joined a study circle that printed and handed out broadsheets on Black history, biblical etymology, and Egyptology in Washington Park. On October 20, 1952, he legally changed his name to Le Sony'r Ra, shortened in practice to Sun Ra, after the Egyptian sun god. He rejected Herman Blount as a slave name and refused for the rest of his life to answer to it.

The band that became the Arkestra assembled in Chicago over the next few years. Tenor saxophonist John Gilmore joined in 1954 and stayed, apart from one break, for four decades. Alto saxophonist Marshall Allen arrived in 1957 and has led the band since 1995. Baritone saxophonist Pat Patrick, bassist Ronnie Boykins, drummer and tape engineer Tommy "Bugs" Hunter, trombonist Julian Priester, and saxophonist Pharoah Sanders all passed through. In the mid-1950s Ra founded the independent El Saturn label with Alton Abraham, a young Chicagoan who became his de facto business manager, booking agent, and archivist. Saturn pressed records in runs as small as seventy-five copies, sold them at gigs and by mail order, and often left off dates, personnel, and even song titles. The first commercially distributed album, Jazz by Sun Ra (later retitled Sun Song), was cut for Tom Wilson's Transition Records on a date the first pressing's label gives as 07-12-56. Super-Sonic Jazz followed in 1957 as Saturn's first LP, and Jazz in Silhouette, recorded in a single Chicago session on March 6, 1959, remains the most admired record of the Chicago years. Around the same time the band adopted the Egyptian robes, sequins, and headdresses that would become inseparable from the music.

Ra moved the Arkestra to New York in the fall of 1961, where the members lived communally so that rehearsals could start at any hour. The Futuristic Sounds of Sun Ra, recorded October 10, 1961 and supervised again by Tom Wilson, came out on Savoy in 1962. In October 1964 he took part in the October Revolution in Jazz, the four-day series at the Cellar Café organized by Bill Dixon that announced the New York avant-garde, and he became a founding member of the Jazz Composers Guild alongside Cecil Taylor, Archie Shepp, Roswell Rudd, and Paul Bley. ESP-Disk issued The Heliocentric Worlds of Sun Ra, Volume One in 1965 and Volume Two the following year, and Saturn released The Magic City, named for Birmingham's own nickname, in 1966. In March 1966 the Arkestra took a Monday-night residency at Slug's Saloon on East 3rd Street that ran regularly for roughly eighteen months and intermittently for five more years, drawing an audience of beat and psychedelic-era listeners along with a share of hecklers. Dizzy Gillespie told him to keep going. Thelonious Monk, hearing the complaint that Ra was too far out, answered that it swung anyway.

When the New York building the band rented was sold in 1968, Ra relocated to a rowhouse on Morton Street in the Germantown section of Philadelphia. It served as the Arkestra's home, rehearsal room, and archive until his death, and was added to the Philadelphia Register of Historic Places in 2022. The band's public profile grew fast: a first West Coast tour in late 1968 with a stage show of twenty to thirty musicians, dancers, singers, and fire-eaters; the cover of Rolling Stone on April 19, 1969; and from 1970 onward near-annual European touring, including the Fondation Maeght nights at Saint-Paul-de-Vence in August 1970 and the Donaueschingen and Berlin festivals that produced It's After the End of the World. In 1971 he served as artist-in-residence at the University of California, Berkeley, teaching a course titled "The Black Man in the Cosmos" whose reading list ran from Egyptian hieroglyphics to the Book of Oahspe, and travelled through Egypt with the Arkestra at the invitation of the drummer Salah Ragab. A distribution deal with Impulse! put a run of Saturn titles into national record stores between 1973 and 1975, among them Jazz in Silhouette, The Magic City, Atlantis, and Fate in a Pleasant Mood, and added two new albums, Astro Black and Pathways to Unknown Worlds. The Afrofuturist feature film Space Is the Place, written by Ra with Joshua Smith and directed by John Coney, was shot in the Bay Area in 1972 and released in 1974.

The last fifteen years brought wider recognition without much softening of the music. The Arkestra played the avant-garde Squat Theatre on West 23rd Street as a house band from the fall of 1979, appeared on Saturday Night Live on May 20, 1978, and worked steadily on European festival stages while Ra kept issuing Saturn LPs in hand-decorated sleeves out of the back of the club. The National Endowment for the Arts named him an NEA Jazz Master in 1982. Late in the decade he recorded a run of well-distributed studio albums: Reflections in Blue and Hours After for Italy's Black Saint, Blue Delight and Purple Night for A&M's Modern Masters Jazz Series, and Mayan Temples for Black Saint again, several of them featuring Don Cherry on pocket trumpet and the singer and violinist June Tyson. He also built a repertoire of Walt Disney songs into the show and recorded "Pink Elephants on Parade" for Hal Willner's 1988 tribute album Stay Awake. A stroke in 1990 slowed but did not stop him, and he handed leadership to John Gilmore when he was too ill to travel. In late 1992 he returned to Birmingham to live with his sister Mary Jenkins, entered Princeton Baptist Medical Center in January 1993 with congestive heart failure, and passed away there on May 30, 1993, at 79. He is buried at Elmwood Cemetery in Birmingham under a footstone reading "Herman Sonny Blount aka Le Sony'r Ra." Gilmore led the Arkestra until his own death in 1995, after which Marshall Allen took over; the band has toured and recorded continuously ever since and earned its first Grammy nomination, for the 2020 album Swirling, more than sixty years after its founding.

Sun Ra spent his entire career refusing the choice between tradition and rupture. He wrote and voiced for a large ensemble the way a swing-era arranger would, keeping Fletcher Henderson's section writing and Duke Ellington's ear for individual tone colors audible inside music that also included collectively improvised noise, tape delay, hand-built percussion, and some of the earliest jazz use of electronic keyboards. He was recording on Wurlitzer electric piano, Hohner Clavinet, and Moog synthesizer years before those instruments became commonplace, and he treated the recording studio itself as an instrument: Art Forms of Dimensions Tomorrow was built around a feedback-and-reverb technique the Arkestra's drummer Tommy Hunter stumbled on while testing a tape machine. His writing ranged from straight blues and standards to the twenty-seven-minute title improvisation on The Magic City, and he insisted on both being the same body of work. He kept his musicians on a communal discipline of daily rehearsal and no drugs, which is why an ensemble of that size could play material this loose without falling apart. The cosmology, the robes, the Saturn origin story, and the endless printed aphorisms were not a costume laid over the music but the frame he built it in, and they made him the founding figure of what later got called Afrofuturism. The spiritual-jazz strain that runs through John Coltrane's final years, Alice Coltrane, and Pharoah Sanders drew on his example, as did the free-jazz circle around Albert Ayler and Cecil Taylor, the artist-run label economics of the 1960s loft scene, and successive waves of experimental musicians from Chicago's AACM to contemporary bands like Apifera in Tel Aviv.