They have been a junior club throughout their existence, with the exception of the 2015–16 season when they competed in Division 2C of the All-Ireland League.

They moved to their present home ground at Mill Road in 1967, having previously played at Ballymascanlon.

[1] The first recorded visit of an established team to the town was that of Wanderers on 8 March 1879, which was played at the Pigeon House Field (a division of the Demesne).

[2] Dundalk were founder members of the Provincial Towns Rugby Football Union in 1882 alongside Armagh, Bessbrook, Derry, and Dungannon.

[5] That season, they reached the final of the (Ulster) Provincial Towns Cup for the first time and were defeated by Dungannon at the Dundalk Athletic Grounds.

The club was revived in 1906 under the presidency of Henry C. Backhouse, adopted colours of black and white striped shirts, and moved to play in Leinster competition exclusively.

[9] They won their first honour in the 1908–09 season when they defeated St Mary's College in a replay to win the Leinster Junior Challenge Cup for the only time.

[21] Dundalk also won the Ryan Midland Cup (a competition run between 1927–28 and 1940–41) twice during this period—in 1934–35 (the first year they were invited to enter) and again in 1936–37.

But the 1937 final became notorious subsequently because the IRFU had attempted to postpone it but apparently did not tell the two teams competing—Dundalk and Birr.

[23] The club moved to its present home ground at Mill Road in 1967 and the official opening came two years later after a £20,000 investment in the pitches and a new pavilion.

It was intended to be an annual inter-provincial tournament contested by Dundalk, Ennis, Lisburn, and Ballina and hosted by each club on rotation.

They lost 10–6 to Lansdowne seconds, which cost them a place in the following season's Leinster Senior League.

[34] The following season, under the New Zealander player-coach, Mark Benton, they won the Nutty Krust Cup for a second time.

Dundalk defeated De La Salle Palmerstown 22–10 to secure promotion, thus becoming a 'senior' club for the first time.

[38] The same season they won the McGowan Cup for the first time since 1993–94 (the competition having undergone several format changes since the formation of the Leinster League),[39] and the All-Ireland Junior Cup for the first time (the club's first national title in its history), defeating Bangor in the final, 55–5.

[9] The colours originally adopted by the club at its first annual meeting in 1878 were royal blue and black.

Since the introduction of shirt sponsorship with the introduction of the Leinster League, the club has been sponsored by several companies with operations in the Dundalk / North Louth region, including: CX+ Sport (a subsidiary of Horseware Ireland), Tony's Pizzeria, Rambo Rugby, Keystone Insurance, Kingspan, Horseware Ireland, O'Callaghan Insurance, Peadar McArdle's Bar, Brubaker's Bar, Duffy Concrete Products, and Heinz.

[9] After being re-established in 1922, the club again played at the Grammar School Grounds then moved to Mount Avenue before the end of the decade.

The official opening took place in September 1969 when the local side played a Wolfhounds XV.

[51] Dundalk have played an annual pre-season friendly against Belfast club Church of Ireland Young Men's Society (CIYMS) R.F.C.

When the two clubs met in an All-Ireland Junior Cup quarter-final in 2013, the trophy was awarded to the victorious Portadown side but plans to renew the annual contest did not materialise.

[54] The Louth Derby is contested between Dundalk and fellow Leinster League side Boyne from Drogheda.