After the First World War, the town of Whitby had two clubs, both playing in the Scarborough and District League, Whitby Whitehall Swifts and Whitby Town. Ever conscious of Whitby’s more illustrious past, the two clubs decided to amalgamate in 1926 as Whitby United. The new club was admitted into the Northern League and the club's name was changed to Whitby Town in 1949.

The club reached a fantastic height in the Amateur Cup days. In 1964 they reached the quarter finals and the following year they made it all the way to Wembley, losing 3–1 to Hendon. The Northern League Cup has been won six times and the North Riding Senior Cup won on five occasions. Whitby were also successful in the short lived Rothman's National Knockout Cup, winning it in 1976 and 1978.

In 1983–84, Whitby came to national prominence when they came back from two goals down to beat Halifax Town 3–2 in the FA Cup first round proper. They were beaten by a late penalty at Wigan in the following round. The same season, Whitby reached the quarter-finals of the FA Trophy for the first time losing to Dagenham in a replay.

In 1992–93, Whitby Town won the Northern League Championship for the first time in their history. Unfortunately due to circumstances completely beyond their control, the club were denied promotion to the Northern Premier League.

In December 1995 the club appointed Harry Dunn as manager. By the end of the season, he had taken Whitby to another Northern League Cup Final victory.
The following season, 1996–97, the Club went from strength to strength. A 0–0 draw against Hull City in the first round proper of the FA Cup, was played at Scarborough on police advice, in a remarkable replay at Boothferry Park, Whitby came from behind to take a 4–3 lead which was held until the dying moments of the game. With only 49 seconds remaining, Hull levelled the score and went on to win 8–4 in extra time. This was to be one of only five defeats in the entire season.

The club came from behind in the Northern League race, winning the Championship in style from neighbours, Billingham Synthonia, before completing an amazing "double" by winning the FA Vase at Wembley, beating North Ferriby United 3–0.

The following season, 1997–98, saw continued success at the Turnbull Ground when the club won the Northern Premier League First Division Championship by a margin of 7 points at their first attempt as well as beating York City 3–0 in the final of the North Riding Senior Cup to become holders for a fifth time.

The 2001–02 season saw Whitby finish in a disappointing 15th in the league, but got to the FA Cup 1st round for the 7th time, only to lose out to Plymouth Argyle after a replay, 3–2. The first game at the Turnbull Ground which finished 1–1 was played in front of the BBC Match of the Day cameras.

Season 2003–04 saw another excellent cup run halted at the hands of Hartlepool United. The Blues put up a spirited showing at Victoria Park but fell 4–0 to an excellent Pools side. Whitby also managed to finish in the play-off zone for the new Conference North but went out on penalties to Radcliffe Borough.

Longtime manager Harry Dunn was replaced by Dave Logan early in season 2004–05 after a string of poor performances. The former Blues stalwart turned the side around as they equalled a club record 19 games without defeat and in the process made the Northern Premier League promotion play-offs. They lost in the semi-final to Farsley Celtic after extra-time.

2005–06 saw Logan looking to improve on that great first season and with the building of the brand-new West Stand at the Turnbull Ground, the future looked bright, though Whitby finished just outside the play-offs, in sixth.

A new era started at the beginning of the 2006–07 season when former Welsh International Lee Nogan took over the reins.

Nogan resigned in October 2007 after an uncharacteristically bad start to the season for Whitby. Senior player Phil Brumwell took temporary command of first team affairs, helped out by Graeme Clark.

The pair were awarded the job on a permanent basis early in 2008 and remained at the helm going into the 2008–09 season. Later, Brumwell resigned to prolong his playing career in December 2008. Clark appointed Nogan as Assistant manager in his second spell on the coaching staff.

Clark resigned in the meantime, and the iconic Harry Dunn began a second spell as Whitby manager. Dunn, who brought a spell of unprecedented success to Whitby, returned to the club on 14 May 2009 and steered Town to a respectable 14th place.

On 4 October 2010, Whitby Town announced that Harry Dunn had resigned as the club's manager, with assistant Bob Scaife, another ex-boss who took Town to their 1993 Northern League title, taking temporary charge of team affairs. Despite overseeing an unbeaten three match spell, Scaife departed by mutual consent.

Former Northern Ireland and Newcastle United player Tommy Cassidy was appointed manager on 20 October 2010. Cassidy left and was replaced by ex-Sunderland stalwart Darren Williams who had only joined the club in August as a player. Williams quickly moved to bring back players who left during Cassidy's reign. Whitby stayed up famously on the final day with a 1–0 victory at Buxton.

Whitby ended 2014–15 in 13th, but after a poor record of 3 wins in 21 league games, Williams was sacked on Monday 23 November 2015.

Chris Hardy was appointed manager of Whitby Town on 3 December 2015, leaving local rivals Guisborough Town. Hardy's first game ended in a 1-0 defeat to Sutton Coldfield Town but results soon picked up, and Hardy led the side to survival, ensuring the job was done with a 2-1 win over Barwell. The following season saw Whitby miss out on the play-offs by two points, finishing 6th.

On 2 April 2019, the contracts of Chris Hardy and Player/Assistant Manager Lee Bullock were extended by two years until the end of the 2020–21 season. However, Hardy resigned in summer 2020, with coach Nathan Haslam joining Bullock as joint manager before Haslam was handed sole rein in September 2022 following the resignation of Lee Bullock.

In the 2023/24 season, Haslam put his name into an elite list of managers at the club as he guided the Seasiders into the First Round of the FA Cup for the first time in 20 years where they were knocked out to Bristol Rovers following a 7-2 defeat at the Memorial Stadium. Silverware was also gained at the end of the campaign as Town ran out 5-1 winners over Boro Rangers in the final of the North Riding Senior Cup at Middlesbrough’s Riverside Stadium.