Mr Cameron and his rival for the leadership, David Davis, had jousted in a good-humoured way and had shown sharp differences in strategy over drugs, taxation and Europe, but the well publicised "head-to-head" confrontation between them failed to come alive until the 57th minute of BBC 1's Question Time.
That was when a man in the audience, a former lecturer, told Mr Cameron: "I have listened to you. You are good on your feet. You are good at waffle and you tell us what you would do, but you don't tell us how."
With ballot papers going out to over 200,000 Tory members today, it highlighted the Mr Cameron's vulnerability to the charge made by Davis supporters that he is "style over substance". While Tory MPs put Mr Cameron, 39, the clear favourite to win, he now has to show the party members that he can fill the policy gaps.
One Davis ally said: "He has got to be able to beat Tony Blair at the despatch box, but one old man in the audience pulled him apart.''
Mr Davis had rehearsed well for the show, being put through questions by Simon Heffer and Amanda Platell and allegedly having speech training to avoid sounding as uninspiring as his speech to the party conference.
The preparation showed as Mr Davis, 57, gained the upper hand by setting out his clear policy proposals, leaving Mr Cameron to say three times: "I agree with David."
Although Mr Davis's tax plans were savaged this week by Danny Finkelstein, a former Tory research director, as "shoddy", Mr Cameron failed to pull them apart. Instead, he insisted that cash available for tax cuts should be shared with higher spending on public services.
Mr Cameron, who had trounced Mr Davis with his speech at the party conference, was confidently expected to eclipse the shadow Home Secretary in the televised debate, but Mr Davis won on points. Mr Cameron's aides played down the significance of his performance saying: "This needed to be a defining moment for Davis and it was not that. We are so far ahead it doesn't matter."
However, the blow to Mr Cameron's image as a slick presenter could do him damage. Mr Davis followed up with a serious blow by comparing Mr Cameron with Mr Blair, who has just endured his worst week in office since the Iraq war.
Viewers could see Mr Davis smirking as Mr Cameron defended his policy strategy, saying: "We have lost three elections in a row. It is obviously tempting in this leadership campaign to try and announce a policy on every single area and give all the detail. That would be a massive misjudgement."
Mr Davis hit back, saying: "This is a fundamental area of difference between us. What you are describing is an approach or strategy taken by Tony Blair. Actually you have been compared to Blair yourself - it was a compliment. But the British public now have seen three Blair Parliaments - they are sick and tired of spin. Frankly, David, this is absolutely the worst moment for the Conservative Party to imitate Tony Blair."
Mr Cameron was cheered when he retorted: "Don't make the mistake of trying to set out policies that will make us look ridiculous in five years' time."
The two also clashed over drugs policy. Mr Davis stood by his promise not to discuss the row over Mr Cameron's refusal to say whether he had taken class A drugs such as cocaine. Mr Cameron said he would downgrade the classification of Ecstasy, which Mr Davis rejected.
One questioner asked both men if they had a "terrible secret" that would embarrass voters if it came out in six months time. Mr Cameron replied: "If there was some terrible secret to come out, I would not be standing here. I would be putting myself forward for this job."
Head to head: the big issues
TERROR - IS 90 DAYS TOO LONG IN DETENTION?
Cameron: "Yes - I think 90 days is a misjudgement. Friends of mine who served in Northern Ireland said internment is a recruiting sergeant for terror. They fear that 90-day detention will have the same effect."
Davis: "I think 90 days is far too long. I think it has to be massively less then 90."
Cameron: "We are in the European Union because we want to trade with our neighbours. We don't want a superstate. But I am realistic. In negotiation you want a clear idea of what you want to retrieve - those powers over employment and social legislation that are doing so much damage."
Davis: "In 1975, we signed up to joining a Common Market not a United States of Europe. What I propose is all those powers should be brought back - environmental powers, social chapter, fishing, agriculture.''
DRUGS - WOULD YOU DOWNGRADE CANNABIS AND ECSTASY?
Cameron: "I had a concern if you put ecstasy and heroin in the same category people don't take it seriously and if you put ecstasy and speed in the same category they won't take it seriously. I said on the Home Affairs committee that is what you would do."
Davis: "Cannabis now is responsible for a large proportion of those who go into psychiatric institutions. I wouldn't downgrade them. It destroys lives. That is why as a parent I was terrified."
Cameron: Supported cuts but said: "I think setting out detailed tax plans five years before you are going to take over the running of the economy simply doesn't make sense because you don't know whether that economy will be growing or shrinking. My worry is that if the Tory party spends too much time flashing up tax cuts, it won't convince people we are serious about managing the economy for the best of everyone in this country."
Davis: "We put tax cuts to the electorate last time three or four weeks before the election. Nobody took us seriously. This is the controversy we have to have week in week out until the next election. The only way we can make that controversy real to people is to show them the size of the numbers involved - we are talking about £1,200 off their tax."Reuse content