Then came what one of his aides calls "the firestorm". The issue of whether he has ever taken drugs, at first no more than an irritant, has grown into a raging controversy now threatening to engulf him.
Last night his team gathered anxiously in his HQ to wait for the first editions of today's newspapers knowing that one serious drugs allegation could send his stellar campaign crashing to earth.
"I had a normal university experience," Cameron told a fringe meeting in Blackpool at the beginning of the month when he was first asked about his drug use. There was little hint then of the danger ahead - after all, several leading Conservatives have openly admitted that they used cannabis, including the current chairman of the party, Francis Maude.
But Kate Moss's recently exposed cocaine use meant the issue of celebrity drug dabbling had additional news currency. Cameron's failure to admit to simply smoking a joint fuelled suspicion he had done more.
By last Sunday it was becoming clear that the issue would not go away. Andrew Marr, interviewing the contender on his 39th birthday, pressed him hard to live up to his image as a modern politician and come clean.
Cameron used the same strategy as before, half-admitting something done a long time ago. "I did lots of things before I came into politics that I shouldn't have done. We all did."
Faced with the massive momentum building behind the youngest contender, his rivals lost little time in seeking to put the bellows beneath the story. Each made clear that they had never taken drugs. Liam Fox - who has most to gain from Cameron's stumble - went furthest. "I have seen too many bright young faces brought into casualty wards with drugs overdoses to take a liberal view," he said.
It was a combination of the David Davis and Kenneth Clarke camps that drove the dagger home on Wednesday at an MPs hustings.
Mark Pritchard, the new Tory MP for the Wrekin, who has given at least £2,000 to the Davis campaign, asked the first candidate Ken Clarke if he had ever taken hard drugs.
The oldest - and wiliest - candidate said it was right to resist personal questions "because it doesn't stop" - but then twisted the knife. Without being asked he said that he had never taken cocaine.
It was the moment the Cameron camp had been dreading - suddenly the issue was not one of a college-room spliff, but something far more politically toxic.
Cocaine, a class A drug, lies at the dividing line between generations of Conservative politicians. Cameron, five years younger than any of his rivals, belongs to a generation - and social class - in which use of the drug is not uncommon.
Profiles of David William Duncan Cameron have tended to dwell on his privilege - the days spent in the hallowed halls of Eton and Brasenose College, Oxford. He has faced criticism for his membership of the Bullingdon Club, a notorious and unashamedly élitist student drinking club, and White's, a London gentleman's club that excludes women.
Then there is the Notting Hill set of influential young Tories, whose youth, metropolitan outlook and class provoke considerable envy among older Conservative MPs. Bound by ties of friendship, social background and the mutual advancement of political ambition, the set provokes envy and curiosity in equal measures among other Conservative MPs.
These are the people who, if he is successful, will inevitably be dubbed "Cameron's Camelot". They include obvious names such as George Osborne, the baby-faced shadow chancellor, Ed Vaizey, the 37-year-old new MP for Wantage, and the Times journalist turned Surrey Heath MP Michael Gove. They are some of the brightest new talents in the 2005 Tory intake. Others in this Notting Hill set are Steve Hilton, his campaign manager, who lives with Rachel Whetsone, an old colleague of Cameron's.
Although there is no suggestion that any take drugs - indeed the last time they met socially they played the board game Risk! - they present a tempting target for opponents.
So too does his family. The fact that he has a seriously disabled four-year-old son, Ivan, has not protected the boy's mother, Cameron's wife Samantha, from intense media scrutiny.
Introduced by her best friend Clare, Cameron's younger sister, "Sam" helps him "keep it real", say friends. She relates that she was brought up near Scunthorpe, was taught to play pool by Tricky, the rap star, as an art student in Bristol and has a tattoo on her ankle.
But as the press has reported, Sam is also the daughter of Sir Reginald Sheffield, a major land-owner, and the step-daughter of Lord Astor. She lists Kate Moss, Stella McCartney, Meg Matthews and Naomi Campbell among her customers at Smythson of Bond Street, an exclusive stationers where she is creative director. She has overseen such innovations as the pigskin baby book (retail price £175) and a new £800 handbag "crammed with secret pockets". A sister, helpfully, is the features editor of Vogue.
Such is the media feeding frenzy surrounding Cameron's drugs past that a reporter from The Times was dispatched to find Tricky, to ask him about whether he had taken drugs with the young Tory MP. (It was a wasted journey to a flat in West Hollywood, as it happens: Tricky refused to speak to the press).
Others, however, have not been so reticent. Rumours began to circulate in Westminster on Wednesday night that Cameron had a close relative in drugs rehab. At least one MP closely associated with a rival camp was seen passing on the "tip" to journalists in the House of Commons. By the time Cameron appeared on BBC1's Question Time the next evening there was a general expectation that he would have to give in to the media pressure. Instead he stuck to his guns. "We are all human and we err and stray," he said.
The Daily Mail was not impressed. In a full-page editorial on Friday it laid into Cameron, insisting that he could not be trusted with the nation's drug policy until he came clean about his own past.
Later that day its sister paper, the Evening Standard, broke the story about the relative it said was now in South Africa after failed attempts to kick heroin.
Still Cameron was not prepared to give in, using an article in yesterday's Mail to counter the suggestion he is "soft" on drugs while again refusing to divulge his own drugs history.
With the prospect of this weekend's Mail on Sunday - Associated Newspaper's third major title - looming, a panicking Cameron team offered a full sit-down interview with the candidate and his wife. Unable to dig the dirt, the newspaper agreed in what appears to be the beginning of an uneasy truce.
Like all political fevers there comes a moment of crisis. That moment is this weekend. Should Cameron survive the efforts of Fleet Street's finest for another 24 hours, the story will move on with the first ballot of MPs on Tuesday.
Until last week one of the main counts against Cameron was that he was untested under political fire. That criticism, at least, has been firmly laid to rest.
Yesterday, Cameron was keeping out of the limelight, waiting to learn his fate at the hands of the media. His aides say that he has grown more, not less, determined to hold the line against the onslaught.
As he gathers his team in the open-plan offices he has leased for the campaign near Victoria Street, Cameron will know the worst is probably behind him. For now.
A Camelot convenes in Notting Hill
As David Cameron faces the roughest storm of his political career this weekend he is drawing strength from a tight-knit circle of friends, family and political allies.
His wife, Sam, 34, and their two children, Ivan, four, and Nancy, 14 months, divide their time between their London home in North Kensington and a cottage in Witney, Oxfordshire.
Nearby in Notting Hill one of his oldest friends, Giles Andreae, has been providing support. A friend since his Eton days, Andreae is a best-selling children's author who has a young family of his own.
Political support and advice is coming from the leading lights of the famed "Notting Hill" set of influential young Conservatives. Michael Gove (pictured right), journalist and MP for Surrey Heath, and Ed Vaizey, MP for Wantage, are helping to staff the campaign HQ in Greycote Street, SW1, while shadow Chancellor George Osborne tours the TV studios.
In the background is Steve Hilton, a Conservative advertising guru who is managing the campaign. Hilton lives with Rachel Whetstone, a friend and ally since she served with Cameron as an adviser to Michael Howard. Whetstone and Cameron fell out recently after reports of her relationship with a member of his wider family.
Campaign funds come from the carpet magnate Lord Harris of Peckham, Simon Wolfson, chief executive of the Next chain, and the Jayroma clothing company owned by Michael Feldman.
MPs AND DRUGS
The following politicians have admitted to having used cannabis while at university
"Did try cannabis while at university, like a lot of students, and it is something that I have left behind."
Told a newspaper he had used cannabis "a long way in the past" and had enjoyed it.
Tried cannabis while studying at Oxford in the 1980s, but found it "absolutely disgusting".
"I tried marijuana, didn't like it particularly and unlike President Clinton I did inhale."
"Nobody is going to die of cannabis and I think it is unrealistic to expect people not to come across it."
Admitted taking cannabis while he was studying economics at Bristol University in the 1960s.
Admitted he had smoked cannabis when he was a student at the University of East Anglia.
Smoked cannabis while a student. "You expect people to experiment. If you don't you haven't been young."
One of seven frontbenchers who admitted cannabis use when matter was raised by Anne Widdecombe
Admitted ahead of the 1997 election that he had smoked cannabis "a couple of times in my late teens".
Another of the group of Tories who confessed to having tried cannabis in the past.
As a youth "had two puffs, didn't like it and have never had any experience of drugs since".
Said he tried cannabis by accident, while a student. Friends mixed some cannabis in with his pipe tobacco.Reuse content