Dalziel, Lanarkshire born centre forward John Miller began his football career with Larkhall Thistle and played for Mossend Hibs, Ardrossan Winton Rovers and Blantyre Victoria before joining Hamilton Academical in September 1915 where he experienced his first taste of senior football, making his Scottish League debut the same month in a match at Falkirk, scoring 4 goals in 8 appearances for The Accies. Miller then served in the Armed Forces with The Glasgow Highlanders alongside his brother Tom during the First World War.
He had a spell at Dumbarton and then joined St Mirren in July 1918 where he played 3 matches for The Buddies. and he then joined his brother Tom in England, scoring 12 goals in 21 matches for Liverpool as a wartime guest in 1918-19 before officially joining Liverpool in July 1919 ahead of the resumption of peacetime football after the end of the First World War, for whom he made his Football League debut against Chelsea that October, making 8 appearances for The Reds during the 1919-20 season, 3 of which were in the same team as his brother.
Aberdeen broke their club transfer fee record to that point to sign Miller in June 1921. He had a superb first season scoring 27 goals in 43 appearances in 1921-22 but then broke his leg the next season, and once recovered he didn’t quite manage to regain his prolific touch in front of goal, joining Partick Thistle in October 1924 after 53 goals in 105 appearances for The Dons. His two years with The Jags were also productive, scoring 30 goals in 53 appearances for Partick Thistle. In April 1925 he had a brief loan with Hamilton to play in a friendly against Liverpool when he one of the scorers in a 3-2 win over the Anfield club, before re-joining Aberdeen in June 1926, where he scored a further 8 goals in 19 appearances before being signed by Clyde for £400 in February 1927, where he managed 4 goals in 8 appearances during the remainder of the season.
Miller joined Dundee later in 1927 and then played for Dunfermline Athletic, joining them in August 1928 and scoring 13 goals in 30 appearances, before heading back to Merseyside to join non league Prescot Cables in 1929. From there he returned to Football League action signing for Third Division (North) club Barrow and their new manager, his brother Tom Miller, in August 1930, where he scored twice in 13 appearances during 1930-31. He finally joined Carlisle United in the 1931 close season but failed to make their first eleven before his retirement from the game.
He was the younger brother of Scottish international Tom Miller, who he played with at Liverpool, and who also played for Manchester United among other clubs, his brothers William and Adam were also footballers, William playing a dozen matches for Hamilton Academical in 1911 in a short career and Adam playing more than 250 matches over a decade for The Accies as well as playing for Royal Albert, St Mirren and Johnstone.