Macaulay was signed by Brentford in October 1946, and made his official Scotland debut (against England at Wembley Stadium on 12 April 1947). By this time he had been converted to a wing half, Brentford were relegated to the Second Division at the end of the 1946-47 season, and he was signed by Arsenal in July 1947 for £10,000. Macaulay made his Arsenal debut against Sunderland on 23 August 1947 and in his first season with the Gunners, he played 40 league matches and won a First Division Championship medal.
He continued to play for Arsenal as a near ever-present for the next two seasons, although he missed out Arsenal's 1950FA Cup triumph after manager Tom Whittaker preferred fellow Scot Alex Forbes in the final. Macaulay left Arsenal for Fulham in June 1950; in all he made 108 appearances in three seasons, scoring one goal. He also won six more caps for Scotland while at Arsenal, bringing his total tally to seven. He spent three season at Fulham, though he could not save them from relegation to Division Two in 1951-52. He moved to Guildford City after that, to become the club's player-manager.
In 1957 he succeeded Tom Parker as manager of Norwich City, where he led the Third Division side to the FA Cup semi-finals in 1959 in one of the most famous FA Cup runs of all time, and promotion to the Second Division the following year. In 1961 he moved on to West Bromwich Albion, though the Baggies did little under his two-year reign, instead enjoying mid-table obscurity.
Macaulay finished his managerial career at Brighton & Hove Albion between 1963 and 1968, leading the club to promotion from the Fourth Division in 1965. After that, he left football management completely, and later worked as a traffic warden. He died in June 1993, aged 77.