Beginning his career in the Premier League with Manchester City, he later played in the top flight for West Bromwich Albion where he was part of the team that had won promotion in 2008 and 2010.

Miller featured regularly in Manchester City's first team pre-season matches in July and August 2006, including a goal in a friendly against Wrexham.

He then proceeded to make substitute appearances in four of Manchester City's first six games of the season, and made his full début on 23 September 2006 in a 2–0 victory over West Ham United, and started the move which led to the opening goal.

On 13 August 2007, West Bromwich Albion manager Tony Mowbray confirmed that he was interested in taking Miller on a season-long loan.

Miller's form during October led to his nomination for Championship player of the month, but the award went to Stoke City's on-loan defender Ryan Shawcross.

[11] On the last day of the January 2008 transfer window, Miller signed on a permanent deal to West Brom on a 3+1⁄2-year contract, for a fee that could rise to £1.4 million.

[14] In December 2008, Miller sustained a serious injury to his knee (cruciate ligament) in a collision with Portsmouth goalkeeper David James and missed the rest of the 2008–09 season.

On 6 August 2011, West Brom manager Roy Hodgson indicated that Ishmael Miller was poised to sign for Nottingham Forest and acknowledged the player's need for regular first team football.

[18] However, although confirming initial negotiations had occurred with West Brom, Forest stressed that there had been no contact or talks at that time with either the player or his agent.

[20][21] West Brom's Sporting & Technical Director, Dan Ashworth, stated: "This move is probably in the best interests of all parties because we can't guarantee Ishmael first-team football and this is a great opportunity for him to hopefully play regularly".

[25] Miller had responded angrily on Twitter to fans' comments and was fined £2,500 by the FA for improper conduct and bringing the game into disrepute.

[28] Miller made his debut for Boro' in their 2–1 victory over Crystal Palace on 25 August 2012, in which he started the game and was eventually substituted in the second half by Luke Williams.

[36] On 6 August 2014, Miller signed a one-year deal with the option of a further year ahead of the season opener against former club Nottingham Forest.

[37] On 2 February 2015, Miller joined Huddersfield Town on a short-term deal until the end of the 2014–15 season, with the option of a further year, taking the number 11 shirt recently vacated by Danny Ward.