The band began when two friends, Jack Antonof and Scott Irby-Ranniar began playing together. They busked in subways and alleyways in New York, and in 1999?2000 recorded a demo that garnered a large degree of record label interest. Despite the array of offers, the duo?calling themselves Steel Train after lyric in a Sublime song?eventually chose to sign with Drive Thru Records. In 2002, the band recorded their debut EP, For You My Dear, recruiting Evan Winiker (formerly of New Jersey pop punk band Random Task) and Matthias Gruber to help with recording and touring. The two later became full members of the band, first Winiker (who was presented as a full member in the promotional pieces for that same EP, released in January 2003) and later Gruber, who joined with second guitarist Matthew Goldman to complete the band and create Steel Train. Together the band went on to record the 1969 EP (a CD of cover versions of songs from that year that inspired the band and their sound), and a year later their debut album Twilight Tales from the Prairies of the Sun, released in 2005. In December 2006 the band announced that they would be parting ways with Matthias Gruber (drums) and Matt Goldman (guitar) who chose to pursue other interests. The positions were filled by tour manager Daniel Silbert on guitar and Jon Shiffman on drums. In 2007, the band released their second full length, Trampoline. Shortly after the release of the record, Scott Irby-Ranniar decided to leave the band. He has since been replaced by North Carolina native Justin Huey.

The band often polarizes opinions, mainly based around the fact that the style of rock they play is more "classic" (Jack often jokes the band was "30 years too late"), yet people see them as very much a part of the emo and pop-punk scene (mainly due to their Drive Thru Records connections). They were well noted for their impressive live shows and "jamming" ability prior to the release of Trampoline.

The lead singer, Jack, also used to date Scarlett Johansson and the song "Better Love" from Twilight Tales from the Prairies of the Sun makes reference to her. Though "Better Love" is a song strictly about her, he also references her in "2 O'Clock", "I Feel Weird" and "Dig": "Josie smiles and laughs, while me and Scarlett will smoke our hash." and "Oh, my scarlet you had a real friend in me." Jack also dated Alia Shawkat of Arrested Development fame in 2008 through mid-2009.

The band has toured nationally with The Format, Silversun Pickups, The Starting Line, The Spill Canvas, Something Corporate, The Early November, The Rocket Summer, The Honorary Title, Robert Randolph and the Family Band, The Hush Sound, Limbeck, Ludo, and Liam and Me.

Steel Train is currently recording their third full-length studio album and is tracking the album's progress on their studio blog, titled "Get Your Shoes Off The Carpet." Although no title has been announced yet, it has been confirmed that the album will have 12 songs, two of which are "Touch Me Bad," and "Soldier in the Army," which were played on their most recent headline tour.

In August 2009, the band left long-time label Drive-Thru Records.

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