Murray, who joined Railtrack from BAA three years ago, left abruptly last week "by mutual agreement".
Steve Marshall, Railtrack's chief executive, will oversee the West Coast Main Line project, the cost of which has risen to £6.3bn from an initial estimate of £2.2bn.
The project came under fire from rail regulator Tom Winsor last week when he questioned the firm's planning and management.
Winsor said: "The West Coast modernisation is the most startling example of a project that has not properly worked."
Murray's other responsibilities will be taken over by investment director Robbie Burns, a former Royal Engineer.
Murray said in a statement that he had enjoyed his time at Railtrack. He said: "The major projects team has achieved a lot, despite some enormous challenges and I believe that the timing is right for me to leave Railtrack for a new challenge."
In a statement Marshall said the requirement of the major project role had moved on and wished Murray well.
Murray earned £175,000 last year.
One Railtrack consultant expressed no surprise at Murray's departure. He said: "I don't think anyone doubts his strategic skill. A lot of what he did was the way the industry should go. It was certain practical levels that were missing in his approach."
Murray, who had been an engineer with Arup, joined Railtrack to lead the construction of the Channel Tunnel Rail Link and to oversee other projects, such as Thameslink.
He promised to create alliances with main suppliers to get away from competitive tendering.
He also said he intended to make performance measures a key part of construction contracts with Railtrack suppliers.
During his time as BAA's head of technical services, Murray was instrumental in bringing in framework agreements designed to improve efficiency at BAA.
Murray is also credited with playing a key role in the development of the government's Rethinking Construction report, published in 1998.