Each region will be run by a separate boss responsible for delivering maintenance and infrastructure renewals.
The sweeping overhaul promises the biggest change in rail infrastructure delivery since British Rail was privatised in 1996.
Former Olympics boss David Higgins, who took over as chief executive just three weeks ago, unveiled the radical changes just weeks before his submission to the official review of rail costs by Sir Roy McNulty, the former chairman of the Civil Aviation Authority.
From April, work will start to devolve power on the first routes in Scotland and Wessex, which matches the lines operated by South West Trains out of Waterloo in London.
Functions due to be transferred cover planning and delivering maintenance, renewals and enhancements, asset management and safety.
Higgins’s plans to have all nine regions operating semi-autonomously within a year.
“We’re devolving accountability to the route level so that we can get closer to our customers and be in a better position to deliver improvements to passengers and freight users, while reducing costs,” said Higgins.
“Each new route managing director will, in effect, be running their own infrastructure railway business with significant annual turnover and resources.
“This represents a significant change of emphasis to give our people on the routes the ability and the means to deliver a bigger, better, more affordable railway. However, we’re determined not to undermine the progress that has been made, but to build on the strengths of what we’ve achieved.
Higgins added: “There will continue to be a critical role for a supporting centre that helps make the most of economies of scale.
“The railway still needs to be planned and operated as a network which operates seamlessly. And we must maintain the company’s focus on efficient and effective management of long-life railway assets.”