Darren Randolph played exclusively with Ardmore Rovers between 1998 and 2003 prior to signing his professional contract with the then Premier League club, Charlton Athletic.

In the last game of the 2006–07 season, Darren made his debut for Charlton at Anfield in a match against Liverpool, which ended in a 2–2 draw.

Darren signed for Scottish Premier League club Motherwell on 1 July 2010. He signed a 3-year-contract at Fir Park and quickly became the club's first choice 'keeper.
He broke the club record of 15 clean sheets and helped Motherwell to the final of the 2011 Scottish Cup. During 2012/13 season, Darren played in the UEFA Champions League with Motherwell.

Darren has represented Ireland at U15, U16, U17, U18, U19, U21 and B levels. On 14 March 2011, he was called up to the full squad for the first time for the game against Macedonia. In May 2011 he was once again called into to the Republic of Ireland squad for the games against Northern Ireland and Scotland in the Carling Cup of Nations.
Darren finally made his full international debut for the senior Republic of Ireland team against Oman in 4-1 friendly win on 11th of September 2012 at Fulham's Craven Cottage.