After playing at the collegiate level for Creighton University, Eric Miller was drafted by the Montreal Impact of Major League Soccer in the 2014 MLS SuperDraft with the fifth pick in the first round. He made his professional debut for the Impact on March 8, 2014 against FC Dallas.
In February 2016, Miller was traded to Colorado Rapids where he went on to appear in 56 games, helping anchor a Rapids defense in 2016 that finished runners-up in the Supporters’ Shield standings.