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Owen Cunningham's playing career spanned over about 10 years, from 1950 to 1960. He played for the Essendon Football Club in the Victorian Football League (VFL), and was a member of their 1952 premiership team. He was also a member of the All-Australian team in 1953. Cunningham was a versatile player who could play in several positions, including full-back, half-back flanker, and centre half-forward.