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Leigh, Lancashire born winger John Millington began his senior football career on the books of Bolton Wanderers in 1933-34, but he didn’t make a first team appearance for The Trotters before joining Third Division (South) Clapton Orient, for whom he made his Football League debut at Coventry City in September 1934. However he made a mere three appearances for the East Londoners before joining Notts County in the 1935 close season. He was on the fringes at Meadow Lane, scoring twice in 16 appearances over his two seasons there, and joined Birmingham in the summer of 1937, where he spent the rest of the year in their reserves without making a first team appearance before transferring to Swansea Town in December 1937. He then played regularly for The Swans over the next 18 months, scoring 7 times in 45 appearances in a struggling Swansea team, before he joined Midland League Scunthorpe & Lindsey United in the summer of 1939. However the onset of the Second World War in September 1939 soon effectively ended his football career.
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