Dundalk have played against several major names in European football such as Liverpool, Tottenham Hotspur, Arsenal, Celtic, FC Porto, PSV Eindhoven, Ajax, Red Star Belgrade, Hajduk Split, Legia Warsaw, and Zenit St Petersburg.

They have faced opponents from the Netherlands most often, having played ties against PSV, Ajax, DOS Utrecht, AZ Alkmaar, and Vitesse Arnhem.

Dundalk play their home matches in Oriel Park, which is a Category 2 Stadium, able to accommodate 3,100 seated spectators for European games.

[6] After having to play the Zurich tie in Dalymount, the installation of floodlighting in Oriel Park ahead of the visit of Vasas SC of Hungary four years later, and the narrow 1–0 defeat that followed, left the town "justifiably proud" at their club's achievement.

A 14–0 aggregate thrashing at the hands of Liverpool in the Fairs Cup a year later, at a time when the club was struggling financially because of sizeable capital debts, remains their biggest defeat in European competition.

In the following season's European Cup they met PSV Eindhoven, and were deemed unlucky to only draw the first leg in Oriel Park.

The Double winning side overcame Linfield in a tie marred by rioting in Oriel Park, which occurred at the height of The Troubles.

[21] Linfield were punished by UEFA for the actions of their supporters by being banned from playing their home-leg in Belfast, and being forced to pay for damage to Oriel Park and Dundalk's expenses for the return leg.

[26] The 1979–80 European Cup run was the subject of a documentary made in 2015 – Once In A Lifetime - produced by Square 1 Productions and broadcast on Setanta Sports on 6 August 2015.

[38] The following season an opportunity was missed against BATE Borisov in the Champions League, when a 0–0 home draw wasn't enough to take advantage of an away goal scored in the first-leg of the second qualifying round.

Dundalk drew Legia Warsaw, with the first leg played in the Aviva Stadium in Dublin in front of a crowd of 30,417.

[43] Defeat in the play-off round meant that Dundalk qualified for the group stage of the Europa League, only the second Irish team to have done so.

[46] In a campaign that would run from 13 July to 8 December, five weeks beyond the end of the domestic season, Dundalk failed to pick up any more points in the remaining matches but the performances of Kenny's team had attracted considerable attention.

[47][48] Following the club's long campaign in 2016, losing to Rosenborg after extra-time in the Champions League second qualifying round tie the following season was a disappointment, even with the financial and organisational disparity between the sides.

[50] But progress that summer was limited when, after defeating Levadia Tallinn and holding AEK Larnaca scoreless in Oriel Park, three quickfire first half goals in the away leg in Cyprus in the 2018-19 Europa League second qualifying round ended their interest in that year's competition.

Their interest in Europe for the season ended there, with a 4–1 aggregate defeat to Slovan Bratislava, which was characterised by the lack of clinical finishing that had dogged the side throughout the campaign.

They were defeated 3–0 in the single-leg tie, which was played at Szusza Ferenc Stadion, Budapest (Hungary) because of travel restrictions related to the COVID-19 pandemic between Slovenia and Ireland.

[55] In the aftermath of that defeat, manager Vinny Perth was sacked by the club and replaced by Filippo Giovagnoli as interim head coach.

[56] Dundalk again dropped into the Europa League and in the second qualifying round faced Andorran champions Inter Club d'Escaldes, winning 1–0.

[58] The victory gave Dundalk a chance to reach the UEFA Europa League group stage for the second time in their history.