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.

The Hawks struggled in their first season in Conference South with manager Darren Freeman blaming the physical nature of some of the teams in the league. After achieving three promotions in four years, Darren Freeman was sacked in January 2014 and replaced by Steve King. King ensured the Hawks retained their place in Conference South on a dramatic last day of the season at the Enclosed Ground against Sutton United, with a late equaliser for the Hawks ensuring a 3–3 draw and an even later penalty by Dover Athletic relegating Hayes & Yeading instead. The club enjoyed their most successful season ever in 2014–2015, finishing fourth in Conference South  and earning a place in the play-off semi finals against Basingstoke Town. After a 1–1 draw at the Enclosed Ground, a tremendous strike from fans’ player of the year Jake Robinson in the second leg won the match 1–0 to earn a place in the final against Boreham Wood, who had finished second in the league. The play-off final at Boreham Wood’s ground finished 1–1 in normal time but an extra time winner for Wood denied the Hawks what would have been their fourth promotion in six seasons. Whitehawk completed the season with a 5–0 victory over Lewes at The Amex to lift the Sussex Senior Cup.

After a good start to the 2015–16 season, The Hawks reached the first round proper of the FA Cup for the first time and achieved national coverage with a 5–3 victory against National League Lincoln City. In the second round The Hawks drew 1–1 at League Two Dagenham & Redbridge, following a dramatic headed goal in added time by Jordan Rose, which was broadcast live by the BBC. In front of a record crowd of 2,174 at the Enclosed Ground, The Hawks lost the second round replay 2–3. To force the match into extra time, Whitehawk again equalised dramatically in added time with a header, this time by Juan Cruz Gotta. The whole match was broadcast live on national TV by BT Sport.

The club submitted a further application to the Football Association to change their name to Brighton City in December 2015. This application was withdrawn a month later after opposition from fans and Chairman John Summers spending time on the terraces at an away game at Chelmsford City.

In February 2016, the club parted company with Steve King after picking up just 9 points from the previous 36 available, a spell which also saw the club fall from 3rd to 13th.Pablo Asensio took over from King as Caretaker Manager, reorganising the squad and playing style to such an extent that after drifting down towards the relegation zone, The Hawks finished the season in style, reaching the play offs for the second season running, with Asensio named manager of the month for April 2016. In the play off semi final against long time league leaders Ebbsfleet United The Hawks lost 1-2 at The Enclosed Ground, but then won the second leg 2-1 in Kent, before eventually losing on penalties after extra time. Pablo Asensio was appointed in May 2016 as permanent manager on a two year contract, which was followed by a complete overhaul of the playing staff for the start of the new season.

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