"[5] His early musical influences include Herb Albert and the Tijuana Brass, Marvin Gaye, Ricki Lee Jones, Queen, Sex Pistols, and The Clash.

[3] Around the age of 22 years, Custer moved to New York City and worked as a session guitarist at the Vision Sound Studios, providing guitar tracks for national television commercials such as Coca–Cola, Ford, Jovan, Mazda, Revlon, and VH1.

[3] Back from New York In 1986, Custer played guitar in the Raleigh area band Four Hard Men with bassist Steev Adams (Pressure Boys, The Hanks), Tony Bowman on keyboards, and Chris Jenson on drums.

[9][10] Another configuration of this group was called Three Hard Men with Custer on guitar, Adams on bass, and Kenny Soule on drums.

[17] One reviewer of The Distance's recordings noted, "Producer John Custer creates a madcap roller derby of ringing guitar riffs" on one track, and "crisp, clear aural onslaught' on another.

[17] Custer also produced a rap song for comedian Rich Hall, his own original music for the WRAL–TV's Rob and Bill's Talk Show, and demo tapes for the Raleigh bands Cry of Love, and Automatic Slim.

[18][19][20][21][5] Custer's first major project was producing the album Blind (Relativity Records, 1991) for the Raleigh punk thrash band Corrosion of Conformity (later COC).

[22][5] Decibel notes, "Allowing the North Carolinians ample space to find their proverbial groove was fledgling producer John Custer.

When Corrosion of Conformity entered Baby Monster Studios in NYC in 1990, they were a full-on heavy metal outfit, and Custer was, to a large degree, the group's sonic tactician.

"[29] COC member Reed Mullin said, "He [Custer ] contributes an enormous amount of stuff that isn't written in the liner notes.

He's like the Daniel Lanois of our little circle and he does not want to put up with that s--t. It's about songwriting, it's about getting the tones on tape and not being scared to take chances.

"[24] In his review of COC's Megalodon, Rob Grissom said, "The legendary and immortal John Custer has once again produced another hardcore masterpiece and seemingly assumes his majestic role as the maestro of the North Carolina music scene.

"[33] Some of Custer's high-profile collaborations for COC projects include working with Warren Haynes (The Allman Brothers Band, Gov't Mule) who played slide guitar on "Stare Too Long," James Hetfield (Metallica) who sang backup vocals on "Man or Ash", and Stanton Moore (Galactic) who played drums on the album In the Arms of God.

[37][22] Cry of Love received a recording contract with Sony (later Columbia) after submitting their demo produced by Custer to the North Carolina Music Showcase in 1992.

[43] With COC and Cry of Love both signed to Columbia, Custer was hired by the label for artist development, giving him what he calls "a pathway to the A&R department".

[3] Custer's hand-picked funk–creation DIG (later DAG) was quickly signed by Columbia because of a Custer–produced a demo tape consisting of just one song.

[42] DAG included drummer Kenny Soul (Nantucket, PKM), along with three members of the Raleigh band Mr. Potatohead: keyboard/vocalist Doug Jervey, guitarist Brian Dennis, and bassist/vocalist Bobby Patterson.

[44][19] DAG origins stem from Custer attending a performance of the Raleigh, North Carolina cover band Mr.

[19] DAG's first release, Righteous (1994) was recorded at Muscle Shoals Sound Studio, with Custer producing, writing or co-writing the tracks.

[3] True to its inspiration of 1970s funk, Righteous featured guest performances by Roger Hawkins of the Muscle Shoals Rhythm Section and jazz trumpeter Jeremy Davenport.

[50] Chris Ford, Gran Torino's lead singer, said the band brought in "hip producer John Custer to improve its sound".

"[51] In 2004, Custer recorded COC's Mike Dean's vocals for the track "Access Babylon" on Probot's self–titled album.

[5] When asked what it was like working with Custer as a producer, BIG Something replied, "It forced us to grow as artists and musicians…It was like getting schooled by a Rock 'n' Roll Jedi master.

"[59] Some of Custer's newest projects include producing the albums for the bands Army of the Dog and The Confessor, both from Raleigh, as well as vocalist Nico Arte.

[5][3] In 2000, Custer created the pop-oriented band Brown with Reed Mullen (COC) on lead vocals and guitar, drummer Marvin Levy (The Veldt), bassist Des White (The Veldt), and keyboardist Michael Thrower (Darkstar),[51] Custer says, "We all play basketball together―that's how this started.

[63] As of 2019, Custer is scoring a movie about a funk band, and working on his own opera that will feature singers from Raleigh choirs.