In a speech on terrorism and security at the International Institute for Strategic Studies, the Conservative leader said: "The two main contenders for the Labour leadership are vying to outdo each other on how 'tough' they can sound on security.
"And today I want to say something directly to Gordon Brown and John Reid: everyone can see what you're up to."
Mr Cameron said: "There is no shame in seeking the leadership of your party, but to use national security for political ends, that is not leadership.
"So let's stop the tough-guy posturing, let's put the national interest first and let's work together to make our country safer."
There is thought to be little love lost between Mr Brown and Mr Reid, who is seen as the last remaining heavyweight who could take on the chancellor in a leadership contest.
While Mr Brown recently pledged to take personal charge of anti-terrorism if - as is still likely - he becomes prime minister next year, Mr Reid has, since taking over as home secretary, coordinated the response to August's alleged airline plots and shepherded in several new crime and anti-social behaviour bills.
Mr Cameron told the audience of academics and security experts: "We must not allow the security of this country to become a political football, either between the parties or within the parties."
That did not mean "avoiding debate or promoting fake consensus", he said, but "it does mean avoiding the temptation to use national security as a political positioning exercise, an attempt to portray one side as being 'tougher' than the other, whether it's one side in a general election or one side in a leadership election.
"A strong and steady approach puts security first, politics second," Mr Cameron claimed. "Putting politics before security leads to an approach that is hasty and hysterical, and that can never be in the national interest."
The Tories oppose ID cards, as well as extending the detention of terror suspects without charge from the current 28 days to 90 days, something Mr Brown has suggested he may try to get through parliament if he becomes leader.
Mr Cameron's speech reiterated his party's commitment to a cabinet-level minister for homeland security, on the American model, although he made clear that the post would operate within the Home Office rather than in a new Whitehall department.
He also called for the immediate banning of Hizb-ut-Tahrir, the radical Muslim group, and more 24-hour security at British ports.
Alongside the creation of a border security force, he said that coastguards must also be given security functions to allow them to board a ship and detain its crew, or the force itself should take that responsibility.
The majority of the prime minister's 12-point plan for combating terror - announced in the aftermath of last year's July 7 bombings - had not been implemented, Mr Cameron said.
Neither had the recommendation of the official 7/7 report that the police should have radio communications between underground train tunnels and street level.
In a further jibe at Mr Brown and Mr Reid, he added: "Today there are, reportedly, two further reviews of security policy under way, one in the Treasury and one in the Home Office.
"I hope the government will explain clearly how these two reviews are working together, what progress we can expect to see and by when."
His comments were seen by some as a reaction to Labour's claims that the crime and terror legislation contained in last week's Queen's speech would "smoke out" Tory weakness on this subject.
