As a player Miller started out his career with Clydebank Strollers before he made the move to Rangers. Miller played for Rangers from 1967 until 1982 before finishing his playing career in Hong Kong. He made 306 appearances during his spell at Rangers and scored 30 goals. After being coached by David White he was promoted to the first team. In the autumn of 1970 he won his first title with the team, the 1970 Scottish League Cup Final. Under coach William Waddell, he was mostly just a second choice player. Therefore, in one of the biggest successes of the club's history, the triumph in the 1972 European Cup Winners' Cup Final, Miller was not on the pitch. It was only after Jock Wallace took over as coach, Miller became increasingly used. As a regular player after the mid-1970s, he won multiple titles. He was something of a legend at Ibrox having played in the 1971 Scottish Cup Final against Celtic despite having a broken jaw.
Miller was appointed as player-manager when he played briefly for South China in Hong Kong in 1983, but was unable to save the club from relegation. He was then briefly manager of Greenock Morton in 1983 before contentiously joining their rivals from Paisley, St Mirren, who were at that time in a higher division.
Miller managed St Mirren from 1983 until 1986. He moulded a side that would win the 1987 Scottish Cup Final, later in the season that he left the club. Miller guided St Mirren to qualification for European competition. One of Saints all-time great nights came in a European campaign when in 1985, Slavia Prague were knocked out after a 3–0 Saints win at Love Street.
He was then manager of Hibernian from 1986 to 1996, through a "difficult" period in the clubs history, as the club came through financial problems. He led Hibs to victory in the 1991–92 Scottish League Cup, beating Rangers in the semi finals (1–0) and Dunfermline Athletic in the final (2–0). Hibs qualified for the UEFA Cup, losing on the away goals rule to RSC Anderlecht. Hibs reached the 1993 Scottish League Cup Final, but this time lost out to Rangers (1–2). Hibs finished the 1994–95 season in third place in the league. Miller was sacked by Hibs in 1996, with some observers accusing him of having betrayed Hibs' "cavalier ideals".
He then moved to Coventry City, accepting an offer from his Scottish compatriot Gordon Strachan to become assistant manager. A year later, unable to resist the challenge of being his own man again, he moved to Aberdeen taking over the manager's post from Roy Aitken. However this stint was not a successful one and he was replaced in 1998 by Paul Hegarty.
Miller joined English Premiership side Liverpool as Director of Scouting under Gérard Houllier in 1999. However, when Rafael Benítez was appointed manager of Liverpool in 2004, he overhauled the scouting system. Miller then subsequently worked as first team coach, helping the club win the Champions League in 2005 and the FA Cup in 2006. Miller left Liverpool in May 2008 to manage Japanese side JEF United Chiba.
Despite taking over the club when they had taken just two points from eleven games, Miller managed to guide the team to safety from relegation. However, following a string of poor results in the next season which the club was in the relegation zone, Miller's contract was terminated by the club in July 2009.
After a year left without commitment, Miller was appointed manager of Swedish team AIK in June 2010 as the successor of Mikael Stahre and the interim solution Björn Wesström. He left in November 2010, after less than five months in charge. AIK had been in some danger of relegation when Miller was appointed, but they eventually finished 11th in the 16-team division.
Miller was appointed head coach of Russian First Division club Sibir Novosibirsk in January 2012. Miller became the first British head coach in Russian football. Miller left the club after just nine matches in charge.
Miller returned to St Mirren on 3 November 2015, as assistant manager to Ian Murray. He became caretaker manager after Murray resigned in December.
Two of Miller's sons, Graeme and Greg, both played for Hibs while Miller was manager there. Miller also employed Greg as a coach while he was manager of JEF United Chiba.Hibernian
Scottish League Cup : 1991–92
Aberdeenshire Cup : 1997–98