Matthew was a teacher and part-time musician until his death in 2016, and helped finance one of Oberst's self-released independent albums.

[9] Shortly thereafter, Oberst began committing his new repertoire to tape in his parents' basement with his father's four track cassette recorder and an acoustic guitar.

In 1994, following a Slowdown Virginia show, Oberst, along with Joel Petersen and brothers Todd Fink and Clark Baechle, formed a band called Norman Bailer, later known as The Faint.

Oberst formed the rock band Commander Venus in 1994 with Tim Kasher, Ben Armstrong, and Robb Nansel.

Kasher left the group to focus on Cursive as they were about to go into the studio to record their second album, and was replaced by Todd Baechle.

Oberst founded Bright Eyes as a solo project in 1995, and after the disbanding of Commander Venus, released A Collection of Songs Written and Recorded 1995–1997 in January 1998.

[12] With the release of 2002's Lifted or The Story Is in the Soil, Keep Your Ear to the Ground, Bright Eyes received national attention and Oberst was proclaimed a breakthrough artist by several notable magazines.

Oberst spent the next two years focusing on other music projects, and in June 2009 told Rolling Stone he wanted to make one final album with Bright Eyes before retiring the group.

In January 2020 the band announced their return to both touring and recording after a nine-year hiatus,[14][15] and released their tenth album Down in the Weeds, Where the World Once Was on August 21, 2020.

[17][18] In November 2007, it was reported that Oberst would work on a solo record with Jake Bellows, and that he and M. Ward would start a band[19] and perform two late December shows in Minneapolis, Minnesota.

Oberst also headlined the Friday night slot of the End of the Road Festival at the Larmer Tree Gardens in Wiltshire, held over the weekend of September 12–14, 2008.

Throughout the end of 2012 and the beginning of 2013, Oberst embarked on a solo tour of North America and Europe performing with Ben Brodin on guitar and vibraphone.

[24] He has been working with producer Jonathan Wilson (Dawes, Father John Misty) and Swedish duo First Aid Kit.

[29] Oberst is one of the founding members of the independent record label Saddle Creek Records, an integral part of Omaha's indie rock scene, which hosts bands such as Cursive, Desaparecidos, The Faint (which left to start its own label Blank.wav), Rilo Kiley (which left to start its own label Brute-Beaute Records), Bright Eyes, Two Gallants, Son, Ambulance, Azure Ray, The Good Life, Sorry About Dresden, and Big Thief among others.

[30] such as Tilly and the Wall, Willy Mason, The Felice Brothers, David Dondero, Taylor Hollingsworth and Jenny Lewis' solo album with The Watson Twins.

[31] Oberst was drawn to music at a very early age, due in part to his brother Matt's penchant for bands like The Smiths, R.E.M., Fugazi, and The Cure.

[33] Joyner wrote the song "Burn Rubber", which Bright Eyes covered on the "Take It Easy (Love Nothing)" single.

Oberst has also been heavily influenced by the 1960s folk revival, mentioning Neil Young, Leonard Cohen, and country singers Emmylou Harris, John Prine and Townes Van Zandt.

He covered Neil Young's "Out on the Weekend", collaborating with Mike Mogis, Jim James and M. Ward in concert.

He performed the Townes Van Zandt song "Rex's Blues" live with fellow musician Steve Earle.

[40] In December 2013, Oberst was accused of sexual assault by a female fan, leading to widespread media coverage.

[43] On October 28, 2015, in the midst of Desaparecidos' tour for their second studio album Payola, it was announced that Oberst had been hospitalized due to "laryngitis, anxiety, and exhaustion," according to a press release.

The entirety of Desaparecidos' remaining tour dates were cancelled and Oberst returned to his hometown of Omaha to recuperate.

[45] On September 27, Bright Eyes cancelled all of their 2024 tour dates following medical tests which determined Oberst "developed a condition that is exacerbated by excessive singing, requiring both treatment and recuperation".

[46][47] The band's second show, in Cleveland, sparked concern from fans after Oberst appeared to be heavily intoxicated and, while slurring his words, expressed frustration with his strained voice and subsequently joked about killing himself.