Upon gaining promotion to the Third Division in 1964 United immediately won the Third Division Championship the following year. In the period which followed Carlisle enjoyed their greatest success outside of cup competitions. Over twelve years the club cemented themselves as a solid Second Division (Then 2nd Tier in English football) side. Within that period Carlisle finished 7 out of 11 seasons in the top half of the table including 3rd in 66/67, 4th in 70/71 and a 3rd in 73/74 which saw them promoted to the top tier of English football. The 71/72 season also saw Carlisle play their only European competition in the club's history, in June 1972 they beat A.S. Roma 3-2 at the Stadio Olimpico in Rome.
Playing in the First Division for the 1974-75 season. Carlisle won their first three fixtures to go top of the English football pyramid, partly due to the likes of Chris Balderstone, scoring the penalty which put them at the top, and Bobby Parker who both went on to make at least 375 league appearances for Carlisle. The success was short lived however, they finished the season in bottom place and were relegated. Highlight victories include doing a double over Everton, and home victories over eventual champions Derby County, and former title holders Ipswich Town, Arsenal, Burnley, Tottenham Hotspur and Wolverhampton Wanderers.
Carlisle still remains the smallest location in England, by local population, to have had a resident top flight football team since 1906. Bill Shankly, an FA Cup and League Championship winning manager by that time, branded Carlisle's climb to the top as "the greatest feat in the history of the game."
Another relegation followed in 76/77 before returning to the Second Division in 1982 under Bob Stokoe. With a team including Malcolm Poskett and Tommy Craig they mounted a promotion challenge in the 83/84 season but finished 7th after a late slump.