In 1952, they beat Merthyr Tydfil 4–3 and became the first non-league side in the modern era to retain the trophy, by defeating Chester City 2–1 the following season.
In 1992, they reluctantly decided to join the League of Wales, but because their application was received too late, they were placed instead in the Cymru Alliance, the second level of the pyramid system.
Over the years, the club have produced players of the highest calibre more than once, including Graham Williams (West Bromwich Albion), Barry Horne (Everton), Andy Jones (Charlton Athletic), Andy Holden (Oldham Athletic) and most recently Lee Trundle (Bristol City) after seeing his career revitalised in his short spell with Rhyl in 2000–01.
Rhyl completed a famous quadruple by rounding off the season with a 6–0 win against Halkyn United in the Final of the North Wales Coast Challenge Cup.
In 2005–06, Rhyl recorded their first-ever win in European competition when they defeated Lithuanian side FK Atlantas 2–1 in the home leg of the first qualifying round of the UEFA Cup.
Rhyl lost the away leg 3–2, but progressed on the away goals rule, the first Welsh team to make the second qualifying round since Barry Town in 1996–97.
A third-placed finish in the Welsh Premier League meant Rhyl would compete for a third year in a row in European Club competitions.
Rhyl's 2006–07 European adventure in the UEFA Cup was ended at the first round with a 2–1 aggregate defeat by Lithuanian side FK Sūduva of Marijampole.
Back in the UEFA Cup in 2007–08, Rhyl achieved a memorable 3–1 home win over FC Haka only to be eliminated on away goals after a 2–0 defeat in the second leg in Finland.
However, their efforts proved futile as Rhyl fell to Partizan with an aggregate score of 12–0, including an 8–0 rout at the Stadion Partizana.
GAP secured promotion to the Welsh Premier League in 2012, having failed to obtain a domestic licence in 2011, leaving Rhyl as potential favourites for the title in 2012–13.
On 6 May 2013, having won the league title on 20 April, Rhyl beat Cefn Druids 2–0, thereby becoming the first club to complete a Cymru Alliance season without a defeat.
In winning 24 matches and drawing 6, Rhyl scored 100 goals and secured promotion back to the Welsh Premier League after an absence of three years.
They were replaced by 24-year-old academy director Niall McGuinness, whose father Laurie, a former Rhyl coach, was appointed as assistant manager.
Working in liaison with the RFA, a ballot was held to decide a name for the new entity, which resulted in CPD Y Rhyl 1879 being formally chosen.
Games between the two clubs often drew crowds of over 1,000 and a few have managed to reach over 1,500 spectators, a great rarity in the Welsh Premier League.