They claimed their first Heineken Cup win on French soil at the Stade Marcel Michelin and, as they became the continent's dominant force, the province's greatest battles have come against the side from the centre of France.
In the next seven days, the 34-year-old captain will face the famous yellow and blue for the ninth and 10th times. His record against them is excellent. He has played against Clermont – for Leinster and Leicester – eight times, losing just once.
The Top 14 side have not lost at home in 50 matches, but Cullen has won at the Stade Marcel Michelin twice. There are not many professionals who can make that claim.
As he prepares to take on the behemoth once again, the Wicklow native recalls all of his personal battles with Leinster's biggest European rival.
Montferrand 20 Leinster 23, Stade Marcel Michelin, December 7;
Leinster 12 Montferrand 9, Donnybrook, December 13
Denis Hickie's last-gasp try secured the Blues' first win on French soil at the seventh time of asking against Montferrand – as Clermont were then known.
Gordon D'Arcy also scored, shipping a hefty late blow from David Bory in the process, before Hickie gave Matt Williams' side a momentous win, thanks, in part, to a certain Kilkenny hurling legend.
Things were no less tense – if a little less entertaining – a week later when Brian O'Meara's late penalty secured the points for Leinster.
"It was a real hang-up for Irish teams going to France in Europe," Cullen recalls.
"It was always a step into the unknown, you didn't really know what it was like and the grounds felt hostile.
"Matt Williams was coach of Leinster and DJ Carey came over with us and gave a speech on the eve of the game. The Kilkenny mantra was to get your retaliation in first in those situations and that was my recollection.
"DJ's big thing was having no fear. His presence around the place was a nice thing at the time... someone from a different sport who everyone respected. It was a good weekend.
"At the end of the game, I remember meeting my parents who were over among a handful of Leinster supporters. It is interesting that now there are 8,000 to 9,000 fans coming from Leinster this weekend. How things have evolved since then is amazing.
"The following week was unusual. I think we thought the work was done and we didn't think that they would turn up, but they came at us. It was an unbelievably physical game at Donnybrook and we just got away with it."
Leicester Tigers 57 Clermont 23, Welford Road, October 22;
Clermont 27 Leicester 40, Stade Marcel Michelin, January 20
Cullen's next meeting with the French side came as they were in a period of flux and barely recognisable from the superpower they are today.
The Tigers hammered the men in yellow in the English midlands, before winning in the French midlands, with Clermont already out of the tournament.
"I think Clermont were in a disrupted period at that stage," Cullen acknowledges. "They had been chopping and changing their coaches quite a few times and, as happens with French teams, their attention was more on the Top 14.
"I wasn't quite sure where their spirits were and certainly in January when we went over there I don't know if their heart was quite in it."
Leinster 29 Clermont 28,
RDS, April 9
The recent rivalry began as the reigning champions hosted the rising force of Clermont and escaped Ballsbridge with the narrowest of wins.
Jonny Sexton was forced off injured, while the visitors were left to rue a disastrous display by Australian fly-half Brock James, who missed a slew of kicks at goal. Leinster went on to lose in Toulouse in the semi-finals.
"I thought we started off the game quite poorly that day," Cullen says. "They got off to a flier, they came out with real intensity and once they get that momentum, they are a hard team to stop.
"Jamie (Heaslip) got two tries to get us back into it, the game just turned for us.
"They were on top at the end, there were missed drop-goals and penalties from Brock James – we have been pretty fortunate against them, it is fair to say.
"That was a relief to be honest, we didn't play particularly well. Even Joe (Schmidt, working for Clermont at the time), it makes him sick to this day how they didn't win that game, because we were well below par that day."
Clermont 20 Leinster 13,
Stade Marcel Michelin, December 12;
Leinster 24 Clermont 8,
Lansdowne Road, December 18
Leinster travelled to France with a backline crisis after Rob Kearney and Brian O'Driscoll were ruled out. With the then untested Eoin O'Malley and Fergus McFadden deputising, they secured a valuable bonus point.
"Like now, it was a six-day turnaround and we had mixed feelings leaving France. There was a realisation that we had got a bonus point and were still in the driving seat in the pool – knowing we had the game the following week, knowing we could step it up. 'Win next week and we can push on'."
A week later, Cian Healy led the way as Leinster secured a surprisingly routine win in their first European game at the newly developed Lansdowne.
"There were a couple of key turning points," Cullen remembers. "We were 10-3 up, they had a maul on our line and they were set really well and we weren't dealing with it. Ti'i Paulo broke off and was stopped short of our line, they had a few pick and goes at our line but couldn't get over.
"Eventually they got penalised for not releasing, we cleared our lines and that took the wind out of their sails a bit.
"I think this Clermont team is stronger than they were two years ago. They have added to their squad, they have some squad of players."
Clermont 15 Leinster 19, Bordeaux, April 29
One of the great European games ended with Clermont centre Wesley Fofana reaching for the line, only to knock the ball on. Leinster escaped Bordeaux with the victory and beat Ulster in the final.
"We rode our luck," Cullen admits. "The first half, we were probably on top in the first 20 minutes but we got a bit sloppy in the scrum and line-out and they got back into the game and we were six down at half-time.
"The pressure was starting to build, but then we hit them for 10 points at the start of the second half and we started to manage territory quite well. But the last six or so minutes turned into a frenzy, they got in the ascendancy and we did a bit of a number on them, thankfully. Again, it was one of those see-saw games that could have gone either way."
And what of this year's double-header? Unlike his international colleagues, Cullen has not had the luxury of distraction over the past month and tomorrow's clash has been looming large on his horizon.
Compared with two years ago, Clermont have the upper hand going into these games, and the Leinster captain knows what lies ahead.
"This year is different because they are two points ahead of us already. There is a slightly different mindset this week.
"There is a lot of pressure on us to win, whereas back then a bonus point was, in reality, not a bad result," the Volkswagen ambassador explained.
"Particularly for me, if you are not involved in those November internationals, these December games are at the forefront of your mind.
"For me, not being involved there, this has been, not all-consuming, but not far off.
"These are the big days, these are what you get excited about and they will define what our season is about."
The more things change, the more they stay the same.
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