Founded in 1945 as Whitehawk & Manor Farm Old Boys, the club joined the Sussex County League in 1952–53 and after finishing third in their inaugural season, were runners-up for three successive seasons from 1954–55, and never out of the top five before changing their name to Whitehawk FC in 1960.

In 1961–62 Whitehawk won the first of three Division One titles. The following season the competition was abandoned due to bad weather, but 1963–64 the Hawks retained the championship, finishing three points clear of second-placed Lewes. The next three seasons however, were nowhere near as successful, and the club found itself relegated at the end of the 1966–67 season, only to make an immediate return as Division Two champions in 1968.

The next nine years saw Whitehawk continue to compete in the top division, until they were relegated for a second time in 1976–77. This time they were to spend four seasons in Division Two, before winning promotion as champions in 1980–81.

In 1983–84 Whitehawk won Division One for the third time, and also enjoyed a good run in the FA Vase before losing at Corinthian Casuals in the 4th Round. 1986–87 saw the Hawks finish as runners-up to Arundel, whilst the club enjoyed by far its best run in the FA Cup in 1988–89, going out in the 4th Qualifying Round to Bognor Regis Town after a replay, having previously drawn at Nyewood Lane. 1993–94 was another good season for the club.

Finishing the season once again as runners-up, this time to Wick; and also having their best ever run in the FA Vase: reaching the 5th Round before going out of the competition to Boston. Hawks won the Brighton Charity Cup for three consecutive seasons in the late 1990s.

Having only finished outside the top three once in the past five seasons, the Hawks have now established themselves as the ‘nearly’ club of the Sussex County League, a title that has also been extended to cup competitions. 2002–03 saw the club once again finish in second place, this time to runaway winners Burgess Hill Town.

A comparatively modest 8th place followed the next season, but in 2004–05 the Hawks regained their position amongst the leading clubs in the League, finishing just a point behind runners-up Rye & Iden United.

The two sides also met in the final of the John O’Hara League Cup and the Hawks emerged as 4–3 winners. However, they were later found to have played an ineligible player in substitute Bertie Foster and therefore Rye United were awarded the trophy.

The Hawks were quietly fancied to do well again in 2005–06 but could only manage 3rd place again behind champions Horsham YMCA and Ringmer. Having been stripped of the League Cup the previous season, their misfortune in cup competitions continued as they reached the Final again, and also the RUR Charity Cup Final, but lost both, to Shoreham and Hailsham Town respectively.

Season 2006–07 began as a two horse race in the eyes of most pundits with Eastbourne Town likely to be the club most likely to deprive Whitehawk of the championship. Despite the Hawks taking four points from the two League encounters it was Town who prevailed by a single point as both finished the season strongly, hoping for the other to slip up.

That Whitehawk finished 11 points clear of 3rd placed Arundel will have been of little consolation. It was a similar story in the domestic cup competitions as the Hawks were beaten once again in the Final of the RUR Cup, this time by Chichester City.

It was another hard-luck story in the FA Vase as well after Whitehawk had fought their way to the quarter-finals and found themselves at home to favourites Truro City. As 1,009 spectators filled the Enclosed Ground, Truro won through with a controversial winner late in the game.

However, the league title success that had previously eluded them, finally came their way in season 2009–10 and with it, came promotion to the Isthmian League Division One South for the first time. Season 2010–11 was their debut season at this level and despite being in the title race for the majority, had to settle for third place and with it, a place in the end-of-season play-offs.

The play-off semi-final ended in disappointment for the Hawks as after a 2–2 draw with Leatherhead at the Enclosed Ground, the Surrey side progressed at Whitehawk’s expense, courtesy of a penalty shoot-out. They completed a league and cup double the following season (2011–12), finishing as league champions and beating Crawley Down 2–1 in the Sussex Senior Cup.

They were promoted to the Isthmian League Premier Division. They had hoped to play the 2012–13 season at the Withdean Stadium but this was blocked by the Football League. The club achieved back to back promotions in the 2012-13 season after winning the Isthmian League Premier Division.

For the 2013-14 season, the club intended to change it’s name to Brighton City, but this move has been put on hold for the time being and the club remains as Whitehawk FC, at least for the 2013-14 season.