John McGrath started his career at Bury from 1955 to 1960. He then spent the next eight years with Newcastle United following a £24,000 transfer, helping them to the Second Division title in 1964-65. In 1968, he joined Southampton for a £30,000 fee, where he would spend the final six years of his playing career, although he also played briefly for Brighton & Hove Albion in 1973.
In total John played 537 league and cup games in a nineteen-year career in the Football League.