When he heard the news on arrival in Farranfore he thought at first he was being wound up. It was incomprehensible to believe that in his first year as a Kerry selector he would be involved in a game that could mark the last managerial hurrah for Mick O'Dwyer, the footballing legend and his father.
A Killorglin-based solicitor and living in Tralee, he has approached today's Thurles showdown without fuss, following a routine perfected in a Waterville household through the years.
However one unknown territory remains. He is unsure as to his heartfelt response to a Kerry victory and the implications that will have for the ending of O'Dwyer senior's 10 year association with the Lilywhites.
While studying law at UCC, John had the misfortune to play in three losing consecutive Sigerson Cup finals with Micko in charge for the first two and Billy Morgan for the third, when he was the captain. And while the Cork university succeeded at their fourth attempt (under Bob Honohan), he had opted out because of the combination of examinations and a back injury.
When it came to making a choice between a possible inter-county career and law, his studies won out.
At local level he attempted a comeback with Waterville after they won an overdue South Kerry championship in 1990, until his back injury worsened and he was forced to retire.
Subsequently, he trained UCC at a time when Karl was involved and Seamus Moynihan was in his first year as a student. After coaching teams at under age level at Waterville, a spell with South Kerry marked the end of his management involvement. For a while at least.
Naturally, football has dominated his life. "I remember Karl saying one time that you had two choices in Waterville, you either played golf or you played football and in our case you played football. If you were Liam Higgins' son you played golf!"
O'Dwyer's break from management was short-lived as he agreed to let his name go forward as the South Kerry representative on the Kerry selection committee at the end of last year. Jack O'Connor had been there, but opted out to work with under-21 team.
John was one of four people nominated and was elected.
His election came in the midst of Kerry's continued post mortem on their defeat to Meath.
"As to what went wrong, or what was wrong, I don't think anybody to this day could put their finger on it," Dwyer recalls. "They talk about staleness, about the difficult of going back a second year, but nobody could be sure what it happened. It was a freak, just one of those things that happened."
This championship campaign set out to prove that fact. The tension surrounding the first round meeting with Limerick was notable as their Shannonside neighbours had recorded a shock win over the Kingdom, midway through the league.
"Regardless of what you might say about the difference between league and championship football, we knew there was going to be a game for us and at the end of the day that was how it transpired.
"Against Cork we felt the game was going away from us until such time as we moved Seamus Moynihan to midfield. Ultimately, either team could have won the game, but I don't think any team should have won it in the conditions. On the day it was a fair result, even though we were lucky to get away with a draw."
Without alluding to the death of death of Michael Ó Sé, the brother of Páidí Ó Sé and father of Darragh, Tomas and Marc, he accepts that from the perspective of the way Cork performed, it was not surprising they triumphed. "They maintained the momentum and achieved a level of consistency which we didn't match. Psychologically, they were very much up for it.
"The day after losing the game I felt it would have been better if we had been knocked out of the championship, but in a matter of a few days the whole mood would have changed.
"I must say that during that period from the Monday to the time we played Wicklow in the qualifier, Páidí's true worth to the team shone through. His motivation skills came to the fore and he seemed to take on a new life. As a result he was immense from that period on."
Playing Wicklow they knew what to expect, but it was different facing up to Fermanagh, who had managed a few good results in the league and who were respected for their championship performances over the last two years. In the event, it was almost a mismatch. "We treated them with the utmost of respect, but the fact that we got a few early goals shattered their confidence."
One week later he was in Croke Park to witness an epic Leinster final. And, it proved to be an interesting experience. In the past, he says he would have been quite nervous watching Kildare games, "about how Karl would have played and how they would have got on", but this time it was quite different.
"This time I was able to sit down and watch the match objectively. I found myself looking at the game more from a selector's point of view than as an actual fan, which was unusual for me. It gave me a basis of objectivity which I thought would not be there. Going to the match I didn't know myself how I was going to react."
And again he saw all the hallmarks of an O'Dwyer trained team.
"They actually came back and had a few right chances from which they might have drawn the game. We would be wary of that from our point of view. I think they will be there right to the finish."
John has been amused by all the media attention over the last week or so. It has had the effect of focusing even more attention on his private dilemma. At the same time, he knows where his priority lies.
For one reason it's a different scenario to 1998, when the teams met in the All- Ireland semi-final and Waterville had Denis O'Dwyer playing on the Kerry team at the time. So, was Maurice Fitzgerald, whose wife Sharon is a first cousin of his. "There was a kind of a rawness about it then, which I don't think is evident now. It was done before when there was much more hype and on the big stage. This game is different because it's an All-Ireland qualifier. But, it's still a big game and Kerry would dearly love to win it."
But how must his father view these things? "The one thing about him, from a point of view of me being involved with Kerry, is that his own attitude towards anything in life is that you gave it a 100% or you didn't give it at all.
"My feeling is that, yes, there are all those side issues. But, at the end of the day, we started last October and I have been involved four or five nights a week, putting in everything that I can put into it. Ultimately, at the end of the day I'd love to see Kerry winning.
"Whatever issues arise after that arise. We'll have to see what happens before we can call the demise of Micko!"
While he doubts his father will get involved at inter-county level again, he cannot envisage a situation where he will divorce himself completely from football. After retiring as Kerry manager in the late 80s, he involved himself with Waterford and likewise for the two year period he opted out of the Kildare job.
"I'm fairly sure he will be looking for some kind of involvement next year!" O'Dwyer says.
The world of Gaelic games sits and waits.