Dumbarton born centre forward John Miller began his football career with hometown professional club Dumbarton in 1891, making his debut in May 1891 at St Mirren, scoring in a 4-2 victory, and scoring in his only other game that season. Miller was then victorious with Dumbarton winning the Scottish Football League in 1891-92, scoring 18 goals in 24 appearances during the season. Following their final game in the season at Abercorn, the Champions for the second year running were welcomed by a sizeable crowd at the station with the D.R.V. band playing Händel’s “See the Conquering Hero Comes”. But Miller headed south to join newly formed Lancashire League club Liverpool that summer, scoring twice on his debut against Bury in September 1892, and after Miller left Dumbarton failed to retain their trophy, only finishing sixth in 1893.
From early on it was clear that Miller was a major coup for Liverpool as Field Sports commented on: “J. Miller is an ideal centre, and no man has earned such high praise as Miller has done since he came to Liverpool. He is a most unselfish player, feeding his forwards with remarkable accuracy, and when a chance of scoring presents itself his shots are sent with a velocity that gives the goalkeeper little chance.” However Miller did turn out to be a goalscoring machine in his only season at Liverpool, scoring 25 goals in 24 games, and wrote his name in the club’s early history books by netting five goals in one game, a 7-0 win against Fleetwood Rangers on 3rd December 1892, a feat only four players at Liverpool have repeated.
Once Liverpool entered the Second Division, Miller wanted a pay rise of £100 down and £3 per week which was a considered an “exorbitant sum” in the papers at the time especially considering every Liverpool player got a bonus for being a resounding success in their local Lancashire League. Miller joined First Division Sheffield Wednesday in June 1893, which the Athletic News concluded “must be paying him a heavy sum”, making his Football League debut against Sunderland scoring both goals in a 2-2 draw in September 1893. Miller scored 8 goals in 13 games for The Wednesday before moving back to Scotland in 1894, playing for Bathgate, Airdrieonians and Clyde during the 1894-95 season before returning to England to join Derby County in the 1895 close season.
He helped Derby to runners up place in the League Championship in his debut season at The Baseball Ground, scoring 17 goals, including 5 in their FA Cup run which saw them lose to Wolverhampton Wanderers in the 1896 FA Cup semi-final at Villa Park. He was again a losing semi finalist the following season, as Derby lost 3-2 to Everton at The Victoria Ground Stoke, finishing 3rd in the League Championship. However he lost his place in the new season and joined Bolton Wanderers in December 1897 after 25 goals in 71 appearances for The Rams. His spell at Burnden Park proved short, he made 9 goalless appearances for The Trotters during the remainder of the 1897-98 season before finishing his senior football career.