Unveiling the government's long awaited aviation white paper, Mr Darling said a second runway at Stansted should be developed in time to open around 2011 or 2012.
"There is a strong case for a third runway at Heathrow once we can be confident that the key condition relating to compliance with air quality limits can be met."
There was little likelihood of achieving this before 2015 to 2020, he told MPs.
To cheers, Mr Darling also ruled out a new airport between Rugby and Coventry in the midlands.
He also announced approval for the expansion of a number of regional airports including Manchester, Newcastle and Leeds/Bradford.
The shadow transport secretary, Theresa May, denounced the announcement as "a fudge from an incompetent government" which will deliver blight to millions of people living around Britain's airports.
Mr Darling stressed that the government remained committed to ensuring that, over time, the aviation industry met the "external costs" to the environment imposed by flights.
The white paper also set out proposals to tackle greenhouse gas emissions and plans for legislation to control noise.
Ministers, he said, had concluded that over the next 30 years there should be two new runways in the south-east.
"The first new runway will need to be completed within a decade, but work also needs to start on planning for a second runway to be built probably around 2015 - 2020.
Ruling out the possibility of a new airport at Cliffe, in Kent, he said Stansted had seen a substantial growth in passengers in recent years and its runway capacity would be used up within a few years.
"A second runway at Stansted would provide very substantial runway capacity in the south-east and generate large economic benefits."
The transport secretary also warned that without additional capacity Heathrow's route network will tend to reduce over time - to the advantage of rival airports in northern Europe.
There was a strong case for a third runway but only if noise and pollution levels could be limited, he said.
"We judge there is a substantially better prospect of achieving this condition in the 2015-2020 period, provided we take action now to tackle the nitrogen dioxide problem."
In the meantime, the white paper set out proposals to increase capacity at Heathrow using existing runways.
Mr Darling disclosed that the government would not seek to overturn the legal agreement preventing construction of a second runway at Gatwick before 2019.
But land would be put aside there in case the conditions relating to Heathrow cannot be met.
He said air traffic remained crucial to Britain's growing economy - with 200,000 jobs directly dependent on aviation and another 600,000 indirectly dependent.
In south Wales, he said, Cardiff should remain the main airport. The government did not see a case for a new airport in south-east Wales.
In Northern Ireland, ministers supported the development of Belfast International airport.
In Scotland, additional runway capacity would be needed in the central belt by around 2020.
Turning to the north of England, Mr Darling said ministers backed development of additional terminal capacity at Manchester and agreed that Liverpool should expand.
In the midlands, the government supported the case for a second runway at Birmingham, subject to strict noise limits, to be built probably around 2016.
Ministers also supported the projected expansion of both passenger and freight traffic at East Midlands airport. "We see no need for a second runway at East Midlands, but will keep this under review," he said.
In the south-west, Mr Darling said he supported the development of Bristol International airport but did not back the option of a new airport north of Bristol.
Responding to Mr Darling's announcement, Ms May said that he needed to strike a "difficult balance" between competing needs.
"That is why the government's decisions need to give clarity and certainty for all involved," she added.
"But far from setting a clear way forward for air transport in the UK, today's announcement is a fudge from an incompetent government which will only deliver blight to millions of people living around airports across this country."
Ms May said that when Birmingham Airport proposed a new short runway, the department refused to issue consultation documents and include the plan in its public consultation.
She warned: "Do you accept that the government's failures in the consultation process now make it certain there will be legal challenges to their decision, thus blighting the lives of millions of people with years of further uncertainty?"
Campaigners today pledged a "vigorous and relentless" challenge to a second runway at Stansted airport.
Norman Mead, chairman of the Stop Stansted Expansion group (SSE), said they would take their campaign to Europe if necessary.
"The idea of a second Stansted runway is illogical and undeliverable," he said.
"The government 'green' credentials are now totally discredited by this white paper whose clear message is 'to hell with protecting the environment, our national heritage and local communities - planes take priority.' Well - we'll see about that."
Councillor Darren Johnson, leader of the Green party group in the London assembly, also attacked the plans: "Aviation is the fastest-growing source of greenhouse gas emissions and we need to be cutting the amount of air traffic, not increasing it.
"Building more runways is totally irresponsible and is in direct contradiction to the government's stated policy of cutting greenhouse gases.
Tony Juniper, the director of Friends of the Earth, agreed: "The government has sacrificed its environmental responsibilities to satisfy the demands of the aviation industry."
However, the white paper was welcomed by the aviation industry. The civil aviation authority (CAA) said it welcomed the "greater clarity" it had brought to discussions about runway capacity.
And British Airways' chief executive Rod Eddington said they "congratulated" the government on recognising the "enormous benefits" that a third runway at London Heathrow airport would bring to Britain.
He said: "For the first time, we have an effective forward-looking aviation policy which recognises Heathrow's key role as Britain's main gateway airport.
"Its continuing development has been guaranteed with terminal five, the opportunity to introduce mixed mode in peak periods and a third runway with a dedicated terminal.
"That is excellent news for the aviation industry, customers, national and regional businesses and tourism."
