ATOC said BT and Ventura had won the five-year deal after an "exhaustive" tendering process.
BT's calls will be answered by their partner Clientlogic at centres in the UK and Bangalore in India, while some of Ventura's calls will go to Bombay.
BT said it would be moving about 250 jobs to India this year.
Around 150,000 people call the rail enquiries number every day.
Under the new contracts - which begin in April - up to half of the calls taken by the enquiries line will be handled in India.
BT, which already takes some of the rail enquiry calls, said that under the new deal it planned to move half of its 500 UK posts to India later in the year.
But, a spokesman added: "It will be as voluntary as possible. As people leave, those posts will shift to India."
But Ventura said the new business would actually result in more jobs being created in the UK.
It said that while it plans to maintain its current 60-40 split between the UK and India for its call centre posts, the firm plans to take on 300 more workers in the UK in the south Yorkshire area to handle the ATOC contract.
However, union Amicus - which has strongly against the trend of firms shifting call centre jobs to India - was not impressed with ATOC's decision.
Amicus general secretary David Fleming said: "Our main concern is why, when firms such as Littlewoods are coming back from India to the UK because of concerns over India, why does ATOC think it makes financial sense to send jobs thousands of miles away?"
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