Howard began his career with the North Jersey Imperials, before making a move to the MetroStars. His appearances soon attracted the attention of English Premier League club Manchester United, who signed him in 2003. He enjoyed relative success with the club, as they won the 2003 FA Community Shield, the 2003–04 FA Cup and the 2005–06 League Cup. After United signed goalkeeper Edwin van der Sar, however, Howard went out on loan to Everton to play more first-team football, and eventually signed permanently with them in February 2007. On January 4, 2012, Howard scored a goal (his first as a professional) against Bolton Wanderers, making him only the fourth goalkeeper to score a goal in a Premier League match. In 2016 Howard made his return to MLS, this time playing for the Colorado Rapids as their starter keeper.