In a speech at the International Institute for Strategic Studies, Mr Cameron said there was "no shame" in seeking the Labour leadership.
But he added: "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."
Tory leader David Cameron has accused Gordon Brown and John Reid of "tough guy posturing" on security, in a bid to boost their own leadership credentials.
In a speech he said the chancellor and home secretary were vying to outdo each other, and urged them to put the national interest first.
Mr Brown is the favourite to succeed Tony Blair when he steps down in 2007, but Mr Reid has not ruled out a bid.
Mr Cameron pledged to work with Mr Blair on counter-terrorism issues.
In a speech at the International Institute for Strategic Studies, Mr Cameron said there was "no shame" in seeking the Labour leadership.
'Let's work together'
But he added: "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."
He urged all politicians to work together to combat terrorism and not allow security to become a "political football".
"That does 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."
Mr Reid has accused the Conservatives of "talking tough, voting soft" on security measures - in particular because of Tory opposition to the government's ID cards scheme.
Mr Reid has criticised Mr Cameron's "hug a hoodie" approach to young offenders, while the chancellor has said counter-terrorism would be his top priority if he was prime minister.
Mr Cameron said counter-terrorism needed "fresh thinking", and he had concerns about the way the current strategy was being pursued.
He said most of a 12-point plan for combating terrorism, announced after the 7 July attacks on London, had not been implemented, nor had all the recommendations of the official 7 July report.
The Tories want to see a dedicated Cabinet level security minister - saying the home secretary's brief is currently too big.
They also want a dedicated border security force to combat people smuggling and coastguards to be given the power to board ships and detain crews.
Mr Cameron also wants the Human Rights Act to be replaced with a British Bill of Rights - to protect UK citizens and allow ministers to deport those who threaten security.
"If our security services believe that a foreign national is a dedicated terrorist and a danger to national security, then the Home Secretary should be able to balance the rights of the suspect with the rights of society as a whole, and proceed with deportation if appropriate," he said.
And he warned his party would take "a lot of persuading" to back moves to extend the limit 28-day limit for the detention of terror suspects without charge or trial.
Attempts to push a 90-day limit through Parliament last year were defeated by a combination of Tory, Lib Dem and rebel Labour MPs, amid fears for civil liberties.
