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The earliest incarnation of Ramsgate FC had played since at least 1886 but folded in 1924, with local rivals Ramsgate Glenville taking over their Southwood Stadium. Glenville did not reform after World War II and a new club dubbed Ramsgate Athletic took over Southwood. The club retained the Athletic name until 1972.

Athletic played in the original incarnation of the Kent League from their formation until the collapse of the league in 1959. This was the club's best period for nearly 50 years, with two consecutive league titles, several county cups, and a run to the first round of the FA Cup. With the collapse of the Kent League the Rams migrated to the Southern League, where they initially did well but were forced to resign and drop down to the re-formed Kent League in 1976.

For nearly thirty years the club performed well without seriously challenging for promotion, but their fortunes changed in 2004 with the return of former manager Jim Ward. He led the club to two consecutive championships (Kent League Premier Division and Isthmian League First Division), taking the club into the Isthmian League Premier Division for 2006–07, which therefore offered the first derby matches for many years against Isle of Thanet rivals Margate. In the club's first season in the Premier Division the Rams finished in 9th place, and followed this with an even better season in 2007–08, finishing in 5th place to reach the play-offs, although they were beaten 2–1 in the semi-final by Staines Town. The Rams also won the Isthmian League Cup, beating AFC Sudbury on penalties at Dartford's Princes Park ground. The following season, however, Ramsgate finished bottom of the table and were relegated.

The 2023–24 season saw Ramsgate reach the second round proper of the FA Cup for the first time in the club's history, defeating National League club Woking 2–1 in the first round to earn a trip to League Two side AFC Wimbledon, who won the match 5–0.