Dennistoun, Glasgow born centre half John Callagher began his football career with St Roch’s in 1920 before joining Second Division Bury in June 1921, making his Football League debut at Blackpool the same September. In 1922-23 he was a fixture in the first eleven making 40 appearances but his opportunities were limited to only 10 games in 1923-24 as Bury were promoted to the top flight as Second Division runners up. Before the end of the season he had joined Southampton in April 1924, but made only one appearance for The Saints when he replaced Alec Campbell for the Second Division match at Stoke City on 1st September 1924. The match ended in a 2-0 defeat and manager Jimmy McIntyre called another new signing, Dennis Jones, into the side for the next match. Callagher spent the remainder of his time at The Dell in the reserves and in the summer of 1925 he was placed on the transfer list at his own request.
In June 1925, he was signed by Wigan Borough for a fee of £400. He made his debut for Wigan in a Third Division (North) fixture at Ashington on 29th August 1925, when he scored in a 3-3 draw. He scored again in the next match, a 5-1 victory over Coventry City in which Tom Fenner scored the other four goals. Callagher retained his place for a further six matches before he lost his place to Bob Scorer without playing again for the club.In June 1926, Callagher joined Norwich City but left after six months without having made a first team appearance and dropped into non-league football playing with Horwich RMI later the same year and Mossley in 1929 before his eventual retirement.