Now Bruton has committed the ultimate nationalist heresy. During a recent speech at the Irish embassy in London, he declared that the 1916 Easter Rising was "completely unnecessary".
As the outraged response shows, this is not just a dry academic debate - it's about how the upcoming centenary could play a crucial role in the 2016 general election.
Bruton's argument is as old as the Rising itself. He points out that in 1916, the British government had already accepted a Home Rule bill to be implemented at the end of World War I.
If Patrick Pearse's hotheads had not jumped the gun, according to Bruton, Ireland could have used Home Rule as a stepping stone to full independence and also avoided a bloodshed.
Not surprisingly, Sinn Fein are leading the rush to condemn Bruton's comments. They insist that Home Rule was a pathetic substitute for true freedom and the British might never have kept their promise anyway.
By this analysis, the Easter blood sacrifice was necessary to strike a blow for liberty and inspire other oppressed nations around the world.
Like most historical 'what if' questions, this one has no right or wrong answer. It is like insisting that if Lee Harvey Oswald had missed, John F Kennedy would have ended the Vietnam War - possibly true, but impossible to prove. In the end, there is more than enough conflicting evidence for both sides to believe what they want to believe.
But the real importance of this debate concerns 2016 as much as 1916.
By an eerie coincidence, the next general election is scheduled to coincide almost exactly with the 100th anniversary of the Rising itself.
Sinn Fein have already made it clear that they will use the commemoration ceremonies to whip up support, just as Eamon de Valera used the 50th anniversary in 1966 to secure his re-election as President.
Essentially, they will try to claim the 1916 Proclamation for themselves and condemn others for betraying Pearse's vision. It may be a crude tactic - but crude tactics have worked for Sinn Fein before.
Enda Kenny's task looks much more complicated. The Taoiseach is known to display a portrait of Michael Collins in his office (John Bruton had a picture of the Home Rule leader John Redmond), but his true feelings about the Rising are a bit of a mystery.
As 2016 approaches, Kenny will come under pressure to say whether or not he agrees with his old friend John. This may be impossible to do without offending at least some voters - because you can argue that one of these conflicts was morally justified, but certainly not both.
While Bruton's speech was undeniably brave, it may also have unwittingly played into Sinn Fein's hands. He implied that the 1916 rebels and the Provisional IRA were cut from the same cloth, a comparison that Gerry Adams would be only too happy to make himself.
Future Shinner leaders such as Mary Lou McDonald will quietly applaud too - because it is much easier to defend romantic idealist James Connolly in the GPO than balaclava-clad thugs on the streets of Belfast.
George Orwell famously wrote: "He who controls the past controls the future. He who controls the present controls the past."
John Bruton's verbal hand grenade shows that the struggle to control Ireland's past is still raging - but at least today we are using words instead of bullets.