In the year 1921 Wrexham were chosen to the newly created Third Division North of the Football League. Their first League match was against Hartlepool United at the Racecourse in front of 8,000 spectators. Playing in blue shirts Wrexham suffered a 0-2 loss. The following week Wrexham gained revenge when they travelled to Hartlepool and earned a 1-0 victory.

In the 1973-74 season Wrexham made it to the FA Cup last eight prior suffering a 1-0 defeat to First Division Burnley. Two years later Wrexham made it to the last eight of the European Cup Winners' Cup before losing to the eventual winners, Anderlecht.

At the termination of the 1977-78 season John Neal departed the club to join Middlesbrough and was replaced by Arfon Griffiths. Griffiths brought Dixie McNeil, Dai Davies and Les Cartwright to the club strengthening the club to such a length that it instantly won the Third Division Championship, reached the last eight of both the FA Cup and the League Cup as well as winning the Welsh Cup.