The firms will design and build the new section of line for alternative link between Oxford and London and the East West Rail scheme to Bedford and Milton Keynes.
The project is overseen by the Bicester to Oxford Collaboration and includes building a new one kilometre section of railway to connect the Bicester Town to Oxford line to the Chiltern main line.
It will also involve widening the existing track bed and building a new station at Oxford Parkway, upgrading Bicester Town and Islip stations and installing a new signalling system.
Once the Oxford to London line and the western phase of the East West Rail scheme is delivered, a further phase will reconstruct and double disused track between Claydon junction and Bletchley and build a new station at Winslow.
The line will be the first new rail link between London and a major British city for 100 years.
Mark Davies, managing director of Carillion Infrastructure, said: “We are delighted to have been selected to deliver this important contract that in itself facilitates two strategically important rail links, one between Oxford and London and another as the first phase of the East West Rail Scheme.”
Mike Kempley, managing director of Buckingham Group Contracting, said: “Over the lifetime of the project we will create new jobs and once complete the project will deliver major improvements to the transport infrastructure across a wide area and deliver significant socio-economic benefits for Oxfordshire and Buckinghamshire.”