Officials told the Sunday Herald: "On average the Borders Railway is forecast to run an operating surplus within ten years, based on our best available estimates of future travel demand and costs."
The Scottish Government agency has revealed passenger estimates of "circa 647,000 return journeys annually (1.29 million single journeys per annum)," adding: "Future demand growth is forecast to increase to 1.078 million return journeys by 2025."
The predictions have been dismissed by the scheme's opponents. Economist Tony Mackay, author of the influential Scottish Economic Monthly Report, calls the project "the next Edinburgh Trams fiasco".
He said: "Most Scottish rail services are already subsidised. I do not believe that the Borders Railway will make a profit."
He added: "There is no doubt that the railway will bring benefits to the Borders. The issue is whether those benefits justify the costs of construction and operation.
"I doubt that the railway will give the boost to local tourism that supporters hope. What would people do if they arrive by train at the local stations? Most tourists would probably choose to travel by car."
But Graham Bell, chairman of the Federation of Small Business in the Borders, defended the new estimates, hinting they should be revised upwards.
"Experience of other reopenings in the UK and Irish Republic suggest the predicted journeys a year on the Borders Railway is likely to be exceeded. The new Limerick-Galway service had more than 30,000 journeys in its first month despite a business case anticipating £2.4m annual losses.
"Also, 18 months after the reopening of the Ebbw Valley line, which was closed in 1962, it had carried a million passengers, originally estimated at 400,000.
"Stirling-Alloa, reopened in 2008 has about 400,000 passengers a year using it, compared with a forecast before rebuilding of 155,000."
Transport Scotland is to release a revised business case for the Borders Railway later this month. The agency claims it takes account of "recent changes in the economy".
The original business case was based on the new line stimulating housebuilding along its route, but was prepared prior to the slump in Scotland's property market.
A spokesman for Network Rail, which assumed responsibility for the line in November, said that preparatory work on the route was "well under way and on-programme."
"The mobilisation for the main works is also now under way, with the first earth works set to begin in spring," he added.