Terry went public with his grievances yesterday and indicated he was willing to raise them at a pre-planned team meeting at their Rustenburg base, even if they upset the Italian.
In the end, having found he had no support amongst his team-mates and having been politely informed challenging Capello was not a great idea, the 29-year-old backed down.
However, the damage was already done and Capello hit back tonight.
"This is the big mistake, this is the very big mistake," Capello told ITV1.
Clearly, Capello is incredulous that his authority should be challenged by a player - his captain until he stripped him of the honour in February over well-publicised personal issues - in a public forum.
"My door is always open. If people want to speak with me they can speak with me," added the Italian.
"Every time we have a meeting I ask the captain, problems? You want to say something? Never.
"Then I read yesterday that John Terry said this, I don't understand why he doesn't speak with me.
"When you speak you have to speak privately, not with the media.
"I think he is more disappointed. I know sometimes players want to speak more with you (the media) than with the other players.
"But the mistake is that you have to speak with the players, with me, with the dressing room."
It has already been suggested Terry was only acting in exactly the same manner he is used to at Chelsea.
Yet the revolving door at Stamford Bridge, that tossed out Avram Grant and Luiz Felipe Scolari amid rumours of dressing room unrest, suggests players have had some sort of power at the west London club.
It seems Terry has discovered Capello's England is a different matter altogether.
Team-mate Frank Lampard may have attempted to damped down some of Terry's criticisms, and praised the Chelsea skipper for speaking his mind.
But for Capello, it was a sign of his authority being challenged.
And that is something he will not tolerate.
So, after one broadside, the Italian turned his attention to Terry's claim that Joe Cole, along with Wayne Rooney, is one of only two players within the England set-up who can unlock a defence.
He did not say so, but it seemed at the time like a demand for Cole's inclusion in Wednesday's do-or-die Group C encounter with Slovenia in Port Elizabeth, when failure to win will almost certainly condemn England to an earlier than expected flight home.
Cole may yet get a game, having been mystifyingly ignored so far.
But Capello has made it clear such a decision will be his alone, and rebuked Terry for singling out one player in a 23-man squad.
"It is another mistake when you speak about one player because there is no respect for the players that play before," he said.
"Always the players think individually, I have to think about the team, it's important. When you speak you have to be careful.
"I respect Joe Cole. But he is one of the 23 players I have here."
That Terry put his dented pride to one side and joined his team-mates on the training ground this morning meant England avoided the kind of cataclysmic confrontation that has beset the French squad this week following Nicolas Anelka's expulsion.
Not that Capello viewed the two situations in anything like the same light.
He said: "No. This was not a revolution. It was one mistake from one player. No more."
Capello did apparently give some ground on Sunday night, agreeing to tell his players his intended starting line-up in advance of his usual policy of informing them five minutes before they board the bus.
But it seems he does not quite see why it is so important.
"After 26 games this is a new problem," he said.
"Before it was okay and the players played well every time. Now they have to know the first XI. I don't understand why.
"In my career I use this system always, why change?''
Capello has exerted his authority in a manner that has left no-one in any doubt who controls this particular ship.
It is widely anticipated the 64-year-old will resign from his £6million-a-year post should England fail to make it through on Wednesday.
With a shell-shocked Terry now firmly put in his place but asked to perform alongside Matthew Upson in Port Elizabeth, huge question marks still remain over the mood in the camp.
But Capello is adamant England can prosper out of adversity.
"Sometimes from a big mistake comes a big performance," he said.
"The next performance will be good. I am 100% sure."