He was signed by Ipswich Town on 22 September 2006 for a nominal fee on a contract until June 2007.[5]
Miller joined League Two side Boston United on a month-long loan in November 2006.[6] This loan at Boston was extended until January 2007.[7] He then joined another League Two side, Darlington, on a month's loan in February 2007.[8] The loan was extended until April 2007,[9] but Miller was recalled in late March to cover for injuries in Ipswich's squad.[10] He made his sole appearance for Ipswich on 31 March 2007, as a substitute in the 74th minute for Jonathan Walters in their Championship fixture in the 3–1 victory over Plymouth Argyle.[11]
Miller agreed a new one-year contract with Ipswich in June 2007 and subsequently re-joined Darlington on an initial month's loan.[12][13] It was extended until January 2008.
Darlington
On 11 January 2008 Miller joined Darlington permanently on a free transfer, signing a one-and-a-half-year contract.[14]
On 10 May 2008, Miller came on as an 87th-minute substitute in the League Two play-off semi-final first leg against Rochdale, replacing the injured Alan White. With the game tied at 1–1, Miller rose to head a 92nd-minute winner from a Neil Wainwrightdirect free kick, to give Darlington the lead heading into the second leg.[15]
After Darlington's players were asked to take a pay cut in November 2011, and Miller did not receive his wages for that month, he handed in his notice and left the club in December 2011.[16]
Grimsby Town
Miller signed a 16-month contract with Conference National club Grimsby Town[17] and made his debut in the starting eleven as the "Mariners" beat Lincoln City 3–1 on 1 January 2012.[18] On 17 February 2012 he scored the equaliser in the 1–2 away victory at Southport, which was also his first goal for Grimsby, a corner from Frankie Artus was met with a powerful header by Miller inside the six-yard box.[19] Miller was ever present for Grimsby during the 2012–13 season and played in the FA Trophy final at Wembley Stadium which ended in a defeat on penalties to Wrexham. The club had also led the Conference for a small part of the season but fell off towards the end and were eventually defeated in the play-offs by Newport County.
Miller was released by the club on 3 May 2013.[20]
Cambridge United
On 3 June 2013, Miller signed for Cambridge United on a two-year deal.[21] At the end of the 2014–15 season the club did not offer him a new deal when his contract expired.[22]
As captain of he led the team to a second-place finish and F.A Trophy glory at Wembley. During the play-off final Miller received a ruptured Achilles' tendon in the final minutes of the game, despite this he still lifted the trophy whilst in a wheelchair as they won 2–1 against Gateshead, sending the club into the Football League. The injury ruled him out for the majority of the next season. After playing very few games he was released on a free transfer.
In August 2017 Miller became a coach at the AFC Sudbury academy.[23] He signed for the club as a player in December 2017.[24] In August 2018, Miller returned to Bury Town as a player-coach.[25]