Born in Glasgow, Darren spent most of early career playing boys club football, but spent a brief period of time at Hearts.
After impressing playing for Knightswood Juveniles, Miller was signed by Albion Rovers but found first team opportunities limited. He joined Irvine Meadow in November 2013. Darren was then signed by Queens Park in summer 2014, playing 34 times for The Spiders and scoring eight goals.
He signed for Scottish Championship outfit Dumbarton in June 2015. After being an unused sub' for the first 4 games of the season, and not even named in the squad for the fifth, he was told he was allowed to leave by manager Stephen Aitken. He left the club on August 28th 2015