The Terrorism Bill, which would allow suspects to be held for up to 90 days without charge, has passed its first stage in the Commons.
Ministers want to hold terror suspects for up to 90 days
Most Conservatives, led by home affairs spokesman David Davis, backed the bill, giving it a majority of 378.
But Mr Davis said the party would oppose the "fundamental sticking point" of longer periods of detention at later stages in the Commons and Lords.
Lib Dems voted against the Terrorism Bill at Wednesday's second reading.
Sixteen Labour MPs, including ex-Cabinet minister Clare Short, rebelled against the government.
Meanwhile, eight Tories - including former chancellor Ken Clarke, who was a candidate to become party leader until last week - joined them.
The Terrorism Bill would outlaw "glorifying" terrorism and make it an offence to commit acts "preparatory to terrorism".
The Conservatives' decision to back the government at this stage of its progress through Parliament signals an end to the previously united approach on the issue by both opposition parties.
David Davis called the case for 90-day detentions unconvincing
The government wants to increase the time police can hold terrorism suspects without charge from two weeks to 90 days.
It says complex cases, often involving detailed research using computers, take more time, making an extension necessary.
Mr Davis told MPs longer detention was "a fundamental sticking point".
Despite talking to police and security services, he had "yet to hear a convincing argument for this measure".
He said the law should change so that terror suspects could be questioned after being charged.
This was a "tiny infringement on our traditions of liberty and justice by comparison with the proposed 90-day extension".
'Weakening common front'
Earlier in the debate, Home Secretary Charles Clarke said: "We cannot properly fight terrorism with one legal hand tied behind our back, or give terrorists the unfettered right to defend themselves as they promote and prepare violent attacks on our society."
He accused the Lib Dems of "knee jerk" opposition and of "weakening the common front of democratic politics against terrorism" by saying they will against the bill.
But Lib Dem home affairs spokesman Mark Oaten replied: "Real opposition and principled opposition is about making a stand on this key issue of holding suspects without charge."
Lib Dem leader Charles Kennedy has said there is no "consensus", even within the government, over some of the bill's "wrong" measures.
His party will be hoping that, without Tory support, enough Labour MPs rebel to force the government to make compromises.