William Henry Marcus Miller Jr. was born June 14, 1959, in Brooklyn, New York, the son of a church organist and choir director; through his father's side he is a cousin of pianist Wynton Kelly. Classically trained on clarinet before he picked up bass, he was working New York's jazz clubs as a session player before he was old enough to drive there, moving through dates with Bernard Wright, Tom Browne, the Brecker Brothers, and Bob James while still a teenager.

That session work led to a run of R&B and pop credits across the late 1970s and 1980s: Aretha Franklin's "Jump to It" (1982, co-written with Luther Vandross), David Bowie's "Underground" from the Labyrinth soundtrack (1986), and, most durably, a run of Luther Vandross singles Miller co-wrote and co-produced, including "Any Love" and "Don't Want to Be a Fool." "Power of Love/Love Power," from Vandross's 1991 album Power of Love, won Miller his first Grammy, Best R&B Song, at the 34th Annual Grammy Awards in February 1992.

In 1980, Miller joined Miles Davis's band, and by the middle of the decade he had become Davis's primary songwriter, arranger, and co-producer. On Tutu (1986), Miller wrote and arranged every track except "Tomaas" (co-written with Davis), "Backyard Ritual" (contributed by George Duke), and a cover of Scritti Politti's "Perfect Way," co-produced the album with Tommy LiPuma, and played most of the instruments himself, including bass, synthesizers, drum machines, bass clarinet, and soprano saxophone. The Davis/Miller partnership continued on the Music from Siesta soundtrack (1987, billed jointly to Miles Davis and Marcus Miller) and Amandla (1989), Davis's final studio album with Miller, dedicated to the memory of arranger Gil Evans.

Miller's solo catalog runs parallel to that studio partnership. He debuted with Suddenly (1983) and Marcus Miller (1984) on Warner Bros., then moved to Dreyfus Jazz for The Sun Don't Lie (1993, dedicated to Davis's memory), Tales (1995), and the live album Live & More (1998). His 2001 album M² stacked guest performances from Herbie Hancock, Hubert Laws, Wayne Shorter, Branford Marsalis, and Chaka Khan, and won the Grammy for Best Contemporary Jazz Album at the 44th Annual Grammy Awards in February 2002. Renaissance (2012) and Afrodeezia (2015) both topped Billboard's Contemporary Jazz Albums chart, with Afrodeezia, inspired by his role as a UNESCO Artist for Peace supporting the Slave Route Project, also picking up a Grammy nomination.

In 1997, Miller assembled a one-off band called Legends for an eleven-date tour of Europe's major jazz festivals, with Eric Clapton, David Sanborn, Steve Gadd, and Joe Sample of The Crusaders. The group never recorded a studio album; its only document is a July 4, 1997 performance at the Montreux Jazz Festival, later released as Legends: Live at Montreux 1997. In 2008, Miller co-founded another supergroup, S.M.V., with fellow bassists Stanley Clarke and Victor Wooten, releasing the album Thunder that year.

Alongside his recording career, Miller has scored more than twenty-five films, from House Party (1990) through Marshall (2017) and Candy Cane Lane (2023). He hosts Miller Time with Marcus Miller on Sirius XM and, as of December 2021, holds a Lifetime Achievement Award from Bass Player magazine. He remains an active touring artist as of 2026.

Miller's catalog runs the crossover jazz arc in both directions at once. As a sideman and songwriter, he moved fluidly between straight jazz session work (the Brecker Brothers, Bob James) and hit R&B/pop production (Vandross, Franklin), often on the same year's calendar. As a bandleader, his solo albums sit consistently in jazz-funk and contemporary jazz, built on his own slap-and-pop bass technique and dense horn-and-rhythm arrangements, while his work behind Miles Davis on Tutu and Amandla shows the same sensibility applied to an elder statesman's late-career reinvention rather than his own name on the cover. Where many crossover artists are described as moving from jazz toward a more commercial sound, Miller spent his most productive years working both directions simultaneously: writing radio hits for other artists' careers while building his own catalog inside jazz's own award categories.