Charlie Hunter was born on May 23, 1967, in Rhode Island and grew up in Berkeley, California. His mother repaired guitars, and the records of his childhood were the folk and blues she had followed as a young woman in Greenwich Village in the late 1950s and early 1960s, among them Reverend Gary Davis and Mississippi John Hurt. He bought his first six-string for $7, took some lessons from the Berkeley guitar teacher Joe Satriani, and has said he has been playing gigs since he was fifteen. At eighteen he went to Europe and worked as a street musician, including in Paris, which he has described as on-the-job training. AllMusic names Joe Pass and Tuck Andress as his primary influences, two guitarists who made one instrument sound like two by folding bass notes into the melody.

Back in the Bay Area he started using a seven-string guitar in 1989, and in 1992 he worked with the San Francisco luthier Ralph Novak on the custom eight-string instrument that became his trademark: three bass strings and five guitar strings, with separate pickups for each half and fanned frets. Some of his first recording credits came with Michael Franti's hip-hop group the Disposable Heroes of Hiphoprisy, where he is credited on guitar and bass on their 1992 album Hypocrisy Is the Greatest Luxury, and then on William S. Burroughs's 1993 spoken-word album Spare Ass Annie and Other Tales, which was made with the Disposable Heroes. The group's tours included dates opening for U2 and Primus. His own Charlie Hunter Trio, with the saxophonist Dave Ellis and the drummer Jay Lane, made a self-titled debut for Prawn Song in 1993, and Blue Note released the follow-up, Bing, Bing, Bing!, in 1995, the first album on which he played the eight-string.

The Blue Note years ran from 1995 to 2001 and produced seven albums under his name. A quartet with Ellis and the alto saxophonist Calder Spanier made Ready... Set... Shango! (1996), and Natty Dread (1997), with Spanier, the tenor saxophonist Kenny Brooks and the drummer Scott Amendola, was an instrumental remake of Bob Marley's album from start to finish. In parallel he led T.J. Kirk with the guitarists Will Bernard and John Schott and Amendola, a band named for the three artists whose music it played, Thelonious Monk, James Brown and Rahsaan Roland Kirk. Its two Warner Bros. albums came out in 1995 and 1996, and the second, If Four Was One, was nominated for the Grammy for Best Contemporary Jazz Performance. Spanier passed away in December 1997 after being hit by a car, and Hunter moved to New York; Return of the Candyman (1998), credited to Charlie Hunter & Pound for Pound with the vibraphonist Stefon Harris, the percussionist John Santos and Amendola, is dedicated to him. That band toured with the New Orleans funk group Galactic, which earned him a following in the jam-band world, and in November 2000 he was on the Blue Note Neon Groove Tour with Soulive and the Jazz Mandolin Project.

Duo (1999) paired him with the drummer Leon Parker, a self-titled album followed in 2000, and in May 2000 he recorded a solo album, Solo Eight-String Guitar, released that August on his own Contra Punto label in a run of 2,000. Outside his own bands, he played bass and guitar on three tracks of D'Angelo's Voodoo (2000), co-writing two of them, including "The Root," and has called it the most challenging session of his career. He also appears on Patricia Barber's Nightclub (2000), on Pat Martino's guitar-duets album All Sides Now (1997), and on John Mayer's Continuum (2006), where he co-wrote and played eight-string on "In Repair." His last Blue Note album, Songs from the Analog Playground (2001), was his first with singers: Mos Def, Theryl DeClouet, Norah Jones and Kurt Elling.

From 2003 he recorded for Ropeadope and others. The Charlie Hunter Quintet made Right Now Move (2003) with the saxophonist John Ellis, the trombonist Curtis Fowlkes and the harmonica player Grégoire Maret; with the percussionist Bobby Previte he began the Groundtruther series, Latitude (2004, with Greg Osby), Longitude (2005, with DJ Logic) and Altitude (2007, with John Medeski); and he was a founding member of the instrumental funk band Garage a Trois with the drummer Stanton Moore and the saxophonist Skerik, appearing on its Mysteryfunk EP (1999) and the albums Emphasizer (2003), Outre Mer (2005) and Calm Down Cologne (2021). His trio resurfaced with Copperopolis (2006) and then Mistico (2007), his one album for Fantasy. Around 2006 he took the top string off the eight-string and settled on a seven. From 2008 he released his own records, among them Baboon Strength (2008), a series of duo albums with Amendola (2012 to 2014), Let the Bells Ring On (2015), the Previte carol album We Two Kings (2015), and Everybody Has a Plan Until They Get Punched in the Mouth (2016) with Previte, the trombonist Curtis Fowlkes and the cornetist Kirk Knuffke.

In 2020 he started SideHustle Records, through which he has released new work and, by his own account, remastered reissues of albums whose rights he regained. The most visible project of the period is SuperBlue, a band with Kurt Elling, the drummer Corey Fonville and the keyboardist DJ Harrison. Its debut album (Edition, 2021) was nominated for the Grammy for Best Jazz Vocal Album, and SuperBlue: The Iridescent Spree (2023) was nominated for Best Alternative Jazz Album. He plays on "Juke Joint" from the drummer Nate Smith's Live-Action (2025), which won the Grammy for Best Alternative Jazz Album in 2026. His 2025 duo album with the guitarist Ella Feingold, Different Strokes for Different Folks, was followed in 2026 by Only a Drop with the singer Lo Steele and the drummer Marcus Finnie (March), Space Bomb with Fonville, Harrison and the bassist Andy Randazzo (June) and AM Clock Radio (September), a trio album with Finnie and the saxophonist Nate Clark. He remains an active touring musician: his own listings run through February 2027, with dates in London in November, Billboard Live Tokyo in January and three nights at the Mondavi Center in Davis, California, in February.

Hunter plays bass lines with his thumb and chords and melody with his fingers on the same instrument, the low strings running to a bass amplifier and the upper strings to a guitar amplifier, and in the eight-string years he paired it with a rotary-speaker simulator to approach the sound of a Hammond organ. His grounding is in the folk, blues, R&B and funk he heard growing up and in the guitar tradition of Joe Pass and Tuck Andress, with Thelonious Monk, James Brown and Rahsaan Roland Kirk as the touchstones of T.J. Kirk and Marley's songbook behind Natty Dread. AllMusic's Sean Westergaard praised him as an agile improviser with a good ear for tone who surrounds himself with excellent players. The funk, blues and rock side is a large part of his work and not a footnote: he has said in interviews that he does not think of himself as a jazz musician, that he loves Motown and sometimes likes Stax more than Blue Note, and that he prefers rhythm, space and the blues to dense harmonic and metric complexity. The jazz side is equally documented: seven Blue Note albums, a Grammy nomination with T.J. Kirk, a duo record with Leon Parker, a guest spot on Pat Martino's All Sides Now, a Groundtruther album with the saxophonist Greg Osby, records built on songs by Monk, Duke Ellington and Cole Porter, and Grammy nominations for SuperBlue as well as T.J. Kirk.