The Cycling Demonstration Towns are Brighton, Darlington, Derby, Exeter, Lancaster and Aylesbury.
A London borough was rejected.
The decision was made by Cycling England, an independent expert body set up by the Department for Transport last March.
Under the scheme, the towns will receive a total of £8.4m government funding over three years and this investment will be matched by the local authority.
Transport minister Derek Twigg said:
"I am delighted to announce the six towns which have been chosen to lead the way in promoting cycling across England and I congratulate Cycling England on the work they have done so far.
"Cycling is a fun, healthy and environmentally friendly way to travel. Research has shown cycling can improve fitness and reduce obesity which can cause serious health problems.
"This investment shows Government is committed to encouraging more people to take up cycling in all or part of their journeys."
Chairman of Cycling England, Phillip Darnton, president of the Bicycle Association, said:
"We want to support towns to work with local schools, hospitals, employers and the wider community to demonstrate the real benefits that cycling can bring: from reducing congestion to increasing levels of physical activity. People want to cycle and we must work together to help them do so more safely and more often."
Cycling England had originally proposed funding for five Cycling Demonstration Towns. However a sixth town, Aylesbury has been included because it is a growth area with the opportunity to plan cycling into a major new programme of development.
From 1st November, five of the towns will each receive £500,000 per year for three years and Aylesbury will receive £300,000 per year over the same period.