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The duo was originally called Charlie Everywhere and used that name to perform around the Saratoga Springs, New York area and to release two EPs on local label Sub-Bombin Records. Upon signing with UK label Barely Breaking Even on January 26, 2009, they changed their name to Phantogram. Carter suggested the name Phantogram when the band wanted to switch from Charlie Everywhere to "something [they] liked". Upon looking up phantogram, they found that it referred to an optical illusion in which two-dimensional images appear to be three-dimensional, and noted parallels between this meaning and their band and music.
Phantogram's eponymous debut EP was self-released on the CE Records label on May 12, 2009, followed in the same year by another EP, Running From the Cops, issued on BBE. They signed with Barsuk Records in October 2009, after encouragement from Erich Cannon of Portland's Spectre Entertainment, who contacted them after he heard songs on their MySpace page. "We were going to write the record, finish it, and release it as a demo for upstate," explained Barthel. "Then our plan was to move down to New York [City] to do the whole networking and meeting people kind of stuff. And we kind of skipped that whole thing, just because of the internet."
Phantogram released their debut album, Eyelid Movies, on September 15, 2009 on BBE (Europe) and Indica Records (Canada), and on February 9, 2010 on Barsuk (US). The album received generally favorable reviews. The album included three singles: "Mouthful of Diamonds", "When I'm Small" and "As Far As I Can See".
In 2010, they enlisted drummer Tim Oakley, formerly of the Mathematicians (where he played under the name Albert Gorithm IV), for their tour. In 2013, the band added guitarist/synth player Nicholas Shelestak to the touring band, while Chris Carhart took over on drums.
The Nightlife EP was released on November 1, 2011. It included the single "Don't Move".
Phantogram appeared on Late Night with Jimmy Fallon in 2011 and 2013; on Jimmy Kimmel Live! in 2014; on The Tonight Show Starring Jimmy Fallon on June 16, 2016; on The Late Show with Stephen Colbert on October 6, 2016; and again on Jimmy Kimmel Live! on December 12, 2016.
The duo collaborated with Big Boi from OutKast on three songs ("Objectum Sexuality", "CPU" and "Lines") from his second studio album, Vicious Lies and Dangerous Rumors, released in December 2012, and were credited as producers for the song "Objectum Sexuality". Phantogram were also featured on the Flaming Lips song "You Lust" from their 2013 album The Terror.
On September 30, 2013, Republic Records released the Phantogram EP, along with the single "Black Out Days". The band's second studio album, Voices, was released on February 18, 2014 by Barsuk/Republic. It included the singles "Bill Murray", 'Fall in Love" and "Nothing But Trouble".
Phantogram have played and toured with the Antlers, Beach House, Metric, Minus the Bear, Caribou, Zero 7, the xx, Ra Ra Riot, School of Seven Bells, Yeasayer, Brazilian Girls, Future Islands and the Glitch Mob. They opened for M83 at the Hollywood Bowl on September 22, 2013. In 2015, Phantogram opened for Alt-J at Madison Square Garden and toured the West Coast with Muse in December 2015 and again during the European leg of the Drones World Tour in April 2016.
In 2015, the band contributed the song "K.Y.S.A" to the Grand Theft Auto V soundtrack; the track appeared in "The Lab" radio station and was also included on the digital and physical versions of the Welcome to Los Santos album. The same year, Phantogram collaborated with Big Boi again, resulting in the seven-song EP Big Grams, released on September 25, 2015 by Epic Records. The EP featured production work from Big Boi, Phantogram, 9th Wonder and Skrillex. Barthel also guest appeared on the Miley Cyrus song "Slab of Butter (Scorpion)" from her album Miley Cyrus & Her Dead Petz.
On May 18, 2018, the band released the single "Someday", backed by a cover of Sparklehorse's "Saturday"; all proceeds from the single were earmarked for donation to the American Foundation for Suicide Prevention.