He toured with a band, though it broke up in his junior year following a serious car accident returning from playing a show at Baylor University.

Before joining Caedmon's Call, he went to community college in Houston for half a semester, and shared an apartment with his older brother who was attending medical school.

[3] Caedmon's Call was formed in 1993 with four original members (three of whom still remain), Cliff Young, Danielle Glenn, Todd Bragg, and Aaron Tate.

Aaron Tate, however, never intended to tour with the band, and was included in a songwriting capacity only, sharing those duties with Derek Webb who also played lead guitar.

Shortly afterward, Webb made the trip to Fort Worth and met future bandmate Cliff Young.

Webb has considered himself a solo act since 2001, but admits his continued collaboration with the band can make it seem like he never left, saying "Caedmon's Call, as it turns out, is very much like hotel california: you can check out anytime you’d like, but you can never really leave.

"[8] On May 22, 2007, it was announced that Webb had again worked with Caedmon's Call, writing and recording for their album, entitled Overdressed, and would be joining the band on their subsequent tour.

[10] One of the songs that was the basis for controversy was "Wedding Dress" where Webb compares Christians who seek fulfillment in things outside of Christ to a person committing adultery.

Another song that generated controversy was "Saint and Sinner" where Webb wrote "I used to be a damned mess but now I look just fine, 'Cause you dressed me up and we drank the finest wine".

In comparison to Webb's previous work, this album has what's been referred to as an "experimental" style to it, and has been compared to the music of Wilco in that respect.

Webb has stated that he tackled these subjects to stimulate discussion and engage people to bring about changes in what he sees as some of the greatest problems the world is facing today.

[17] On May 12, 2009, Webb sent a message to his email mailing list stating that his next album Stockholm Syndrome was deemed too controversial for his record label to release.

[19] On September 29, 2017, Webb released Fingers Crossed which was promoted as "a deeply personal tale of two divorces," touching on themes of his marriage ending and his loss of faith.

[21][non-primary source needed] On April 7, 2023, Webb released The Jesus Hypothesis, an album about finding meaning and beauty and exploring issues of gender identity and sexuality.

Inspired by that realization, Webb helped form NoiseTrade, a website that allows users to download music for free from independent musicians.