Born in Grange-over-Sands, Lancashire, Crayston started his career at Division 3 North Barrow in 1928, spending two seasons there before moving to Bradford (Park Avenue), where he developed into a strong, dependable and aerially powerful right-half.

Crayston's move to the big-time came when he was signed by Arsenal in 1934, and he scored on his competitive debut in an 8-1 thrashing of Liverpool. Crayston became a regular in the Arsenal side straight away, winning the League Championship in 1935 and 1938 and the FA Cup in 1936.

Like many of his contemporaries, the Second World War robbed Crayston of what should have been the peak of his career; he joined the Royal Air Force whilst still playing irregular wartime football. Unfortunately, a serious knee injury in a wartime match against West Ham in 1943 forced Crayston to retire from playing. He played 207 matches in total, scoring 17 goals. He also won 8 caps for England between 1935 and 1937, scoring one goal.

After his premature retirement and demobbing from the RAF, Crayston moved into coaching, and in June 1947 he became assistant to new Arsenal manager Tom Whittaker. After Whittaker's untimely death in 1956, Crayston became full manager. However, his stewardship of the team was brief and unsuccessful; unable to bring any new players in, the team started to decline. In 1957-58 Arsenal slipped to 12th in the League (their worst position for 38 years) and faced a humiliating Cup defeat at the hands of Northampton Town. Disillusioned, in May 1958 he resigned as Arsenal manager, and took up the reins at Doncaster Rovers a couple of months later, holding the post until his retirement from the game in 1961. He died in 1992, at the age of 82.