Greenock, Renfrewshire born inside left James Miller began his football career with Blantyre Victoria from where he signed for St Mirren in June 1917, scoring 3 goals in 16 appearances for The Buddies before signing for hometown club Greenock Morton in September 1920. He signed for Third Division (North) club Grimsby Town in the 1921 close season, making his Football League debut at Ashington, scoring a hat-trick in the return fixture a week later at Blundell Park on his home debut. Miller scored 14 goals for Grimsby in his debut season as they finished third in the Third Division (North), second top scoring to Jimmy Carmichael, and scored 11 goals the next season.
He had scored a further 11 goals in 1923-24 when he was signed by Second Division club Manchester United for £500 in March 1924 after 36 goals in 98 appearances for Grimsby Town, and he scored for United in a 1-1 draw at Hull City, his second of four matches for United before losing his place in April. He didn’t stay at Old Trafford and joined Midland League club York City in the summer of 1924, moving to Boston Town in July 1925. He subsequently played for Shirebrook in 1927 before his eventual retirement.