However, the club in its present form dates back to 1949 when they joined the newly re-organised Welsh National League (Wrexham Area) as Ruthin British Legion.

1979–80 was a big season for the club as both the first team and reserves were promoted back to the first and second divisions both as champions of their respective leagues.

A decade of stability ensued with the three senior teams establishing themselves in their respective leagues with their youth system being set up in 1986.

This youth system was to be the making of the club providing a consistent source of players for the senior teams.

As the second tier of Welsh Football comes under the wing of the FAW in 2019 Ruthin have been one of the longest-serving clubs in the Huws Gray Alliance along with Buckley Town.

On 27 August 2021 Ruthin played hosts to Guilsfield F C, kick off 7.45pm, for their first game under newly installed floodlights and with refurbished player facilities.

In March 2024 Manager Phil Hudson left the club and assistant Dave Evans was asked to stand in until the end of the season.