Carlisle United won their first game in the Football League Third Division North with the side of Prout, Coulthard, Cook, Harrison, Ross, Pigg, Agar, Hutchison, McConnell, Ward and Watson beating Accrington Stanley 3-2. Their next game was played against Hartlepool United and still stands to this day as their record victory at 8 goals to nil.
When the Second World War began in 1939, Carlisle United withdrew from national and regional competitions and only played local football. When the war was over the club returned to the Football League and appointed Ivor Broadis as player-manager, making him the youngest league club manager in history. He then had the distinction of becoming the first manager to transfer himself when he moved to Sunderland, he continued to live and train in Carlisle. Broadis returned to Carlisle United in 1955 an ex-England international.
In 1949, the club became the first to appoint Bill Shankly as manager. Shankly, a former player at Carlisle, later went on to manage local rivals Workington (helping them finish above Carlisle for the first time) before being appointed as manager of Liverpool in 1959; over the next 15 years he would guide the club to numerous trophy successes. It is at Carlisle where he met local player Geoff Twentyman, who he would later sign as head scout at Liverpool, and lifelong friend Ivor Broadis. Broadis, who was playing for Sunderland but living and training with Carlisle, once arrived late for training and Shankly asserted that he would play by United's training rules even if he didn't play there. According to Shankly, he said to Broadis: "What do you think you're doing? Who do you think you are? If you do the training we do you can train with us and we'll play five-a-side and you'll run your guts out as an example to everybody else".
Carlisle were members of the Third Division North until 1958 when it combined with the Third Division South to become the Fourth Division. They remained there until 1962 when they won their first promotion, they were relegated the following season but immediately bounced back to begin the most prosperous period in the club's history.