The former Foreign Secretary, who backed the 2003 invasion, sat stony-faced as Ed Miliband declared at the party's Manchester conference that Labour was "wrong to take Britain to war and we need to be honest about that".
David Miliband's anger boiled over when Harriet Harman, Labour's deputy leader, joined the applause for his brother's attack. "You voted for it, why are you clapping?" David asked her in a remark picked up by an ITV News microphone.
"I'm clapping because he is the leader. I'm supporting him," Ms Harman replied.
The incident may prove to be the final straw as David decides whether to remain in the Shadow Cabinet after his narrow and painful defeat by his younger brother on Saturday. Political allies yesterday maintained the pressure on him to stand in the election among Labour MPs. But his wife, Louise, is understood to be urging him to return to the backbenches.
Last night his close colleagues admitted that the arguments of those urging him to stand down had been strengthened by the clash with Ms Harman. They have warned him that the media would constantly be looking for splits between him and his brother if he remained on Labour's front bench. "It proves the point," one adviser said. "David has given his life to politics since his early 20s. He doesn't want to give it up, but this illustrates perfectly the problem with staying in the Shadow Cabinet. He's in an impossible position."
Labour MPs said Ed Miliband's decision to criticise the Iraq war had closed off one of David's options – remaining as shadow Foreign Secretary. Ed was not in Parliament at the time and disclosed his opposition to the war during the leadership election.
David must make up his mind by 5pm today, when nominations for the election close. He is likely to remain MP for South Shields and intends to be active in politics – and to support Labour under his brother's leadership.
Ed Miliband told the conference: "Iraq was an issue that divided our party and our country. Many sincerely believed that the world faced a very real threat. I criticise nobody faced with making the toughest of decisions and I honour our troops who fought and died there. But I do believe that we were wrong... Wrong because the war was not a last resort, because we did not build sufficient alliances and because we undermined the United Nations. America has drawn a line under Iraq and so must we."
The Iraq controversy overshadowed an impressive first conference speech by Labour's new leader and he appeared to have won over the doubters.
He portrayed himself as the leader of a new generation of optimists and painted David Cameron as a pessimist who is using the public deficit as a smokescreen for cuts, saying: "You were the optimist once, but now all you offer is a miserable, pessimistic view of what we can achieve. And you hide behind the deficit to justify it." In contrast with Mr Cameron's "big society", he outlined his vision of a "good society".
Although he criticised his former boss Gordon Brown on the economy as well as Tony Blair on Iraq, Mr Miliband sought to quash speculation that he would shift his party to the left and allow it to live in a "comfort zone". Promising strong leadership, he told his party: "It won't always be easy. You won't always like what I have to say. This country faces some tough choices. And so do we. And we need to change."
After trade unionists secured his victory over his brother, he tried to send a message to the unions that strikes over spending cuts could alienate the public: "That is why I have no truck, and you should have no truck, with overblown rhetoric about waves of irresponsible strikes. The public won't support them. And you shouldn't support them either."
His tough message upset some union bosses. "Rubbish,"shouted Len McCluskey, assistant general secretary of Unite.
He said he believed strongly in the need to reduce the deficit, saying his party needed to win back its fiscal credibility. "There will be cuts and there would have been if we had been in government. Some of them will be painful and would have been if we had been in government."
Promising not to oppose every cut the Government proposes, he warned his party: "There will be some things the Coalition does that we don't like as a party but we will have to support. And come the next election there will be some things it has done that I will want to reverse but won't be able to."
But he also gave himself room to take on the Coalition over the cuts. "What we should not to is make a bad situation worse by embarking on deficit reduction at a pace that endangers our economic recovery," he said." No plan for growth means no credible plan for deficit reduction." His strategy, he said, would be to shape the "centre ground"– not allow it to be dominated or defined by Labour's opponents.
New leader's policy vision
Spending cuts
"I am serious about reducing our deficit... I won't oppose every cut the Coalition proposes... But what we should not do is make a bad situation worse by embarking on deficit reduction at a pace that endangers our economic recovery."
This formulation is designed to help win back Labour's credibility on the economy while giving Mr Miliband some wriggle room to amend Alistair Darling's policy to halve the deficit over four years. Critics will accuse him of trying to have it both ways.
Low pay
"I believe not just in a minimum wage but the foundation of our economy in future must be a living wage."
A future Labour government could force employers to pay a "living wage" of about £7.60 an hour, rather than the minimum wage of £5.80 an hour. The move would be opposed by employers, but Mr Miliband will point out that their warnings about huge job losses before the minimum wage was introduced proved unfounded.
High pay
"The gap between rich and poor does matter. What does it say about the values of our society, what have we become, that a banker can earn in day what the care worker can earn in a year? Responsibility in this country shouldn't just be about what you can get away with."
Mr Miliband supports a High Pay Commission to investigate the gap between top and bottom pay levels in the private and public sector.
Welfare
"There are those for whom the benefits system has become a trap."
Mr Miliband will oppose "arbitrary" benefit cuts proposed by the Coalition. But he is sympathetic to "tough and tender" reforms drawn up by James Purnell, the former work and pensions secretary, which were not supported by Gordon Brown.
Crime
"When Ken Clarke [the Justice Secretary] says we need to look at short sentences in prison because of high re-offending rates, I'm not going to say he's soft on crime."
Mr Miliband's support for Mr Clarke's "prison isn't working" approach marks a break with New Labour's tough stance on crime.
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