He joined Manchester United as an associated schoolboy at the age of 14, and was an FA Youth Cup finalist in 1982.

He was given his debut for United on 16 May 1984 by manager Ron Atkinson, in their 2–0 league defeat against Nottingham Forest at the City Ground. He made a solitary league appearance the following season, although in 1985–86 he scored three goals in 12 league games, but he did not get a serious run in the side until the 1987–88 season, by which time Alex Ferguson was United’s manager, when he played 22 league games and scored three goals. 1988–89 saw Blackmore enjoy even more first team opportunities as he played 28 times in the league.

He won 39 caps for Wales. He made his senior debut for the national side on 26 February 1985, in a 1–1 friendly draw with Norway, and his final appearance for the Welsh side came on 29 March 1997.

In 1991, he won a European Cup Winners’ Cup medal with United, and in 1990 he won the FA Cup with them. He was United’s regular left-back in the 1990–91 season, but when Paul Parker signed in the close season, Denis Irwin was switched to left-back and Blackmore returned to his familiar pattern of alternating between different positions, although he did enjoy a good run at right-back when Parker was injured.

He joined Middlesbrough on a free transfer for the 1994–95 season after spending more than a decade at Old Trafford. He was signed by newly appointed player-manager Bryan Robson, who had just headed to Teesside from United. He helped them win promotion to the Premier League as Division One champions in his first season on Teesside, playing in 30 League games and scoring two goals. He also appeared in Middlesbrough’s 1997 FA Cup Final defeat by Chelsea. Whilst at Boro he had a loan spell with Bristol City.

On 3 September 2018, Clayton Blackmore enters the coaching staff of Dynamo Brest Academy. The contract is signed until March 2021.