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Although the first recorded football match in Whitstable was in 1885, the first record of Whitstable Town's existence was the following year. After a couple of years playing in a field behind the railway station, the club relocated to The Belmont Ground in 1888, where they play to this day.

In 1909 the Oystermen joined the original Kent League, where they played until it folded in 1959, winning the Division Two title three times. They also lifted the Kent Amateur Cup (now Kent Senior Trophy) in 1929. After the collapse of the Kent League, the club played for a while in the Aetolian League, but this meant long trips to play London teams as opposed to the earlier money-spinning East Kent derbies, and this was a period of financial struggle for the club, which dropped into the amateur leagues for a number of years.

In the late 1960s the Kent League reformed, with the Oystermen among the founder members. They also attracted national publicity in 1989 when striker Gerry Allen scored a goal after just 4 seconds of a match.

They had remained members of the Kent League until their promotion to the Isthmian League in 2007. The 2006–07 season marked the best in the club's history when supporter Tony Rouse took over as chairman from long time servant of the club Joe Brownett. Rouse appointed first team captain Marc Seager as the club's manager taking over from Matt Toms. Under Marc Seager's leadership the team won the Kent League and the Kent Senior Trophy. In 2012 former local referee Gary Johnson took over as chairman from Joe Brownett (after his second spell in the chair) but in 2015 Johnson was replaced once again by Joe Brownett (his third spell as chairman).

Whitstable spent nine seasons in the Isthmian League Division One South with a best placed 8th finish in the 2014–15 season. This is the highest level in the football pyramid that the club have played. Relegation at the end of 2015–16 season was followed by two seasons in the Southern Counties East Football League Premier Division with Scott Porter as manager.

Under manager Scott Porter the successful 2017-18 campaign resulted in a 2nd-place finish to Sevenoaks Town, good enough to secure promotion back to the Isthmian League, as well as two cup final victories. The first season in the newly formed Isthmian League South East division resulted in 12th place, the club's 2nd best finish at this level. In June 2019 the club merged with Whitstable Town Junior Football Club with ownership moving to a limited company with Steve Clayton as chairman and Lloyd Blackman taking over as manager from Porter. Whitstable were relegated to the Southern Counties East Football League at the end of the 2021–22 season.