McCombs joined Eleventh Dream Day around 1985, replacing original bassist Shu Shubat, and has remained a member ever since. The band earned acclaim for their blend of punkish energy and Neil Young-inspired rootsiness, and a short-lived stint on Atlantic resulted in a pair of minor hits on alternative rock radio. McCombs and drummer John Herndon had the idea of establishing a Sly Robbie-like rhythm section, and the two co-founded Tortoise (initially known as Mosquito) along with drummer John McEntire and bassist Bundy K. Brown, soon joined by percussionist Dan Bitney. The band's unconventional, rhythm-heavy lineup and incorporation of influences such as cool jazz and minimalism made their sound stand apart from most rock bands, and their willingness to remix and rework their material opened up a portal of possibilities. While active with Tortoise and Eleventh Dream Day, McCombs played in similarly exploratory groups such as the For Carnation, Toe, Pullman, and Boxhead Ensemble, and played on records by Stereolab, Yo La Tengo, the Aluminum Group, Calexico, and others.
McCombs initially formed Brokeback as a solo venture, releasing a pair of 1997 singles before Thrill Jockey issued the 1999 debut full-length Field Recordings from the Cook County Water Table, which featured contributions from several of his bandmates in Tortoise as well as Stereolab's Mary Hansen, cornetist Rob Mazurek, and double bassists Josh Abrams and Noel Kupersmith. 2000's Morse Code in the Modern Age: Across the Americas featured musicians such as guitarist Alan Licht and Yo La Tengo's James McNew. Looks at the Bird, Brokeback's slightly more electronic third full-length, appeared in 2003. In 2009, Thrill Jockey released Sycamore, an improvised collaboration between McCombs and David Daniell. Versions, a Bundy K. Brown-mixed assemblage of material from the same sessions as well as two live gigs, followed in 2012. Brokeback and the Black Rock, the band's first album in a decade, appeared in 2013, with James Elkington, Chris Hansen, and Pete Croke part of the revamped lineup. Illinois River Valley Blues was released in 2017, featuring drummer Areif Sless-Kitain. In 2022, McCombs issued his first solo album, a set of textural explorations titled VMAK