Mr Darling, Transport Secretary from 2002 to 2006, said he had changed his mind on HS2 because of the rising cost - originally £30 billion, which has leapt to nearer £50bn, and which some reports place at over £70bn. "My principal concern is if you spend this money on this one railway line, you will not have the money that you need to spend on maintaining and upgrading existing lines like the East Coast Mainline, the line to Bristol, the commuter lines and so on.
"My experience as Transport Secretary is if you do not spend money on upgrading the track and improving the trains, the thing will eventually start falling apart as it did by the mid-1990s."
When the example of the Scotland to London West Coast Mainline was raised, Mr Darling replied: "There's a good example. For 30 years, successive governments did not spend the money that they needed to spend on it. It was an absolute disaster; long delays and so on."
The Edinburgh MP, who is leading the campaign against Scottish independence, noted how the proposed spend by Railtrack on the West Coast line of £14bn was scaled back to £8bn but stressed how this was the sort of money that needed to be spent on the railways to maintain them.
"The East Coast Mainline, which was last done up seriously, probably 25 years ago, will need money spent on it...That's my concern; we are spending a lot of money on something that still isn't finalised and I also question we would get the gains claimed for it."
Mr Darling also questioned the focus on London and south-east England, stressing how the connections between Britain's other cities were not good and that while there was talk of bringing HS2 to Scotland, there were still no plans to.
"My fear is if you build this visionary project, you have a nightmare in the rest of the network because you don't have the money to spend on it," he added.
Labour officially supports HS2, which will be a major infrastructure project, creating hundreds of thousands of jobs. But recently, Ed Balls, the Shadow Chancellor, said there must be no "blank cheque" for a scheme, which will see 225mph trains running between London and Birmingham by 2026. A second phase to Manchester and then Leeds is due by 2033.
In response to Mr Darling's concerns, Patrick McLoughlin, the Transport Secretary, insisted there was investment planned for other lines and that cross-party support for HS2 remained strong, including from Labour.