The deal will include significant re-signalling of both Aviemore and Pitlochry stations which will see the historic semaphore signals replaced with colour lights.
In addition, work will be delivered in partnership with platform extensions at Pitlochry and the extension of the double track section to the north at Aviemore station, while three private level crossings near Pitlochry will be upgraded as well as further work at Inverness, Kincraig and Slochd.
The scheme is part of an overall £57m Scottish Government-funded investment in the line linking the Highland capital and the Central Belt. This phase of work is scheduled to be complete next March, ahead of the introduction of the new timetable in May 2019.
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Transport Minister Humza Yousaf said: "The awarding of a further contract for work on the Highland mainline is another important milestone in this Scottish Government funded project, which is on track to complete in spring 2019.
"The signalling works between Inverness and Perth enable far more efficient crossing of trains, which combined with infrastructure enhancements, will contribute to delivering faster and more frequent journeys between Inverness and the Central Belt."
Matthew Spence, Route Delivery Director for Network Rail, said: "Upgrading the signalling on the Highland mainline is vital to deliver more and faster trains on the line, improving stopping patterns and providing better connectivity for customers.
"We will work throughout to deliver in the most efficient and cost-effective way possible while minimising disruption for both lineside communities and passengers."
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