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The club was founded in 1908 as Cambridge Town F.C., as Cambridge had not been granted city status at that point, and were committed to amateur sport. The club competed in the Southern Amateur League, developing a fierce rivalry with Ipswich Town that was evident both on and off the pitch. In 1912 they won the Challenge International du Nord in 1912, beating US Tourquennoise 4-1. The club were invited to join the newly formed Eastern Counties League in 1935, but declined the invitation and switched instead to the Spartan League.

The resumption of football after the Second World War saw Cambridge Town continuing in the Spartan League, winning the competition 3 times between 1945 and 1950, before joining the Athenian League for the 1950–51 season. Cambridge was formally granted city status in 1951. Both Cambridge Town and their neighbours Abbey United applied to change their name to Cambridge City. Cambridge Town's application was approved because it arrived first and therefore Abbey United changed their name to Cambridge United. In 1958, 22 years after turning down the chance to apply to the Football League, Cambridge City joined the Southern League South Eastern zone as a professional club. The club went on to make five applications to join the Football League between 1959 and 1974, all of which were unsuccessful.

In the late 1950s and 1960s Cambridge City commanded the highest attendances in non-league football, regularly attracting average gates in excess of 3,500 (higher than rivals United during that period) and occasionally attracting gates over 10,000. ^[] They were Southern League Champions in 1962–63 and stayed in the League's top division until 1968, when they were relegated and turned semi-professional. They were promoted back to the Premier Division after finishing in the Division One runners-up spot in 1969–70, and finished second in their first season back in the Premier Division.

Cambridge United were elected into the Football League in 1970, and from that point City struggled to attract as many supporters to their games as their cross-city rivals – by the early 1980s, when United were enjoying a prolonged spell in the 2nd Division, City were attracting fewer than 200 supporters to each game.^[] 1975–76 saw the second relegation in the club's history, into the Southern League's Division One North. They remained there until 1979–80, when a re-organisation of the league's structure, in order to become a feeder to the newly formed Football Conference, placed City in the Midland Division. A switch was made to the Southern Division in the 1982–83 season and this seemed to coincide with a turn around in City's fortunes, and 1985–86 saw City win the division on goal difference and gain promotion back to the Premier Division. The late 1980's through to the early 90's saw City competing at the top of the Premier Division.

City suffered a last day relegation at Atherstone United in May 1996, only to be reprieved. After a few seasons struggling at the wrong end of the table, including another reprieve from relegation in 1999, City's league form improved at just the right time and the club joined the Football Conference's newly formed South Division in 2004–05, embarking on a successful FA Cup run in the same season – following United's relegation from the League in 2005, the two Cambridge clubs were only one division apart. However, the club was encountering financial difficulties and the club's City Ground was sold to an Isle of Man company called Ross River, which was linked to Brian York, a man who had briefly been a director of the club. The then board announced that it was to scrap the first team and make the reserve team into a feeder for Cambridge United. This prompted the formation of a supporters' trust, who within weeks had taken over the running of the club. The club took Ross River to court, where it was ruled that the club were victims of fraudulent misrepresentation and bribery – the former chief executive Arthur Eastham having taken a £10,000 payment from Brian York. though the original deal was not overturned.

In May 2008 City were demoted from the Conference South, after their ground failed an FA inspection, to the Southern League Premier Division for the 2008–09 season. They were moved into the Isthmian League Division One North for 2019-20, before switching to the Northern Premier League Midlands Division for the start of the 2021/22 season, where they continue to be members.