[3] The first local derby between Holywell and their fierce, long-time rivals Flint occurred on 27 November 1880, with the Holywellites edging the "very interesting game" by a single goal from J.C.

[4] During the early history of the club, Holywell played their football on a ground known as Ffordd Fer ('Short Way'), which was a short distance from the town centre and located near to where the local high school is now situated.

Alas, Holywell failed to appear for their scheduled cup match in early January 1893 and were thrown out of the competition by the FAW, thus awarding the fixture to their opponents.

[18] It was during this period when Holywell United hosted their biggest game at that time, playing a friendly match against Everton XI at their Ffordd Fer ground.

On both occasions, United took on Newport-based side Lovell's Athletic in the finals held at Newtown and Flint respectively, and lost both fixtures by a 0–2 scoreline as their opponents won two of their three consecutive cups.

Twelve months later, they would return to the NWC Amateur Cup final, for the ninth time, to defend their trophy against a strong Porthmadoc side at Bangor.

It was also during the same season that the record attendance for a Holywell game was set in 1962 when 3000 spectators packed into Halkyn Road for a 1961-62 Welsh Cup sixth-round tie with Swansea Town.

[21] The club continued to earn silverware during that period when they successfully defended their Clwyd League Premier Division title in the following season, winning it for the second time in a row.

Holywell Town were selected to become founder members of the Cymru Alliance in 1990–91, the top-tier league for northern and central Welsh football clubs at that time.

However, the reality of competing in the Welsh top flight was starting to seriously affect the club's finances, and as budgets were cut, results further diminished in the League of Wales.

Even though they had been relegated for the first time from the League of Wales, Holywell Town's initial exile away from the top division was a brief period as they rebounded back in the 1997-98 season.

Their reappearance in the League of Wales became a nightmare for the club as Holywell Town finished rock bottom of the 1998-99 table and suffered a second relegation from the LoW in three seasons.

It was at that point that the club decided to part company with their Manchester-based manager and squad in favour of a more local set-up in order to improve performances on the pitch.

[21] Thankfully for the club, Holywell Town narrowly avoided relegation to the third tier despite their lowly finish as the league was short of its full complement of teams.

Holywell Town initially struggled to compete within the Welsh Alliance League, finishing in the bottom half of the table for their first three seasons at the third tier.

Holywell won their first piece of silverware in thirteen years, when they sensationally came back from 0–2 down in the 89th minute, to win the prestigious FAW Trophy for the very first time by beating Conwy United 3–2 at the neutral venue of Belle Vue, Rhyl.

In the penultimate game of the 2011–12 season, a 1–3 defeat to title rivals, Holyhead Hotspur,[23] ensured that the Ynys Môn-side snatched top spot and promotion away from the Wellmen, by a winning margin of just a single point.

For the start of the 2012–13 season, Mike Thomas was replaced as Holywell manager by their club captain, Johnny Haseldin, who adopted a player-manager role.

Victories over Cymru Alliance sides Penrhyncoch, Penycae, and Porthmadog were achieved, and most famously a fourth-round 3–2 win over Newtown, who would subsequently in fifth position in that season's Welsh Premier League, ensured the club faced another WPL team in Aberystwyth Town at the neutral venue of Latham Park, Newtown for the semi-final fixture, and it was shown live on the Welsh-language channel of S4C.

Despite taking the lead after just eight minutes through midfielder Tom McElmeel, and giving an incredibly valiant effort throughout the game, the Wellmen lost the tie 3–1.

[40] Despite the loss, they wrapped up the league title with three games remaining by beating Llanrwst United 3–0,[41] and finally earned themselves promotion back to the Cymru Alliance for the 2015–16 season.

The highlights of the league campaign were the incredible home victories against Llanfairpwll and Pwllheli where the Wellmen inflicted a heavy defeat on the Anglesey side of 15–1,[42] and beating the Llŷn Peninsula team 10–0.

A brace from Phil Lloyd, a goal from Steve Thomas, and a Sam Jones penalty secured Holywell's victory over the Gwynedd-based side.

Under the continued management of Johnny Haseldin, they also reached two North East Wales FA (NEWFA) Challenge Cup finals, but lost 0–2 to Cefn Druids in 2016,[46] and 1–2 Ruthin Town in 2018,[47] respectively.

Unfortunately throughout the season, and prior to the games in April, Holywell had only managed to earn themselves a further three wins between October and March, although one of those victories was a confidence-boosting 2–1 result in the Boxing Day derby against Flint Town United.

[54] What made it even more gut-wrenching to Wellmen supporters was that Penrhyncoch were losing with ten minutes remaining in their final match of the season, before scoring two late goals against Conwy Borough to confirm a 3–2 victory and escape relegation, thus condemning Holywell to third-tier football once again.

They managed to clinch the WNL Premier title and gain promotion back to the now-named Cymru North, albeit on a superior points-per-game (PPG) ratio after the Welsh football season was halted and concluded due to the COVID-19 pandemic that was affecting the country at the time.

The Wellmen also progressed far into the Welsh League Cup defeating Colwyn Bay, Conwy Borough, and Prestatyn Town to reach the quarter-finals of the competition.

[63] Holywell Town currently plays at the Bartons North Wales Stadium, located on Halkyn Road (Welsh: Ffordd Helygain).

In recent times, the Halkyn Road ground has been dramatically improved, such as increasing parking facilities and better water drainage, and the stadium has been the venue for many Youth International fixtures.