A report published by Transport Scotland has found that it will now cost £1.5 billion for the five improvement projects: Aberdeen to Inverness Improvement Project, Edinburgh to Glasgow Improvement Programme, Highland Mainline Improvement Project, Shotts Electrification and Stirling, Dunblane, Alloa Electrification.
Transport Minister Humza Yousaf told the Committee that he had confidence in the rail improvement plan.
But asked about the role of Ministers had in holding contractors to account, he declared Ministers had to rely on Network Rail's estimates, and then conceded to not being a transport expert.
Rural Affairs Committee member Jamie Greene MSP said:
"The Transport Secretary this morning claimed he had full confidence in the rail improvement programme - and yet we now learn that costs have sky-rocketed by nearly £400 million.
"It's not good enough to blame Network Rail for everything.
"Coming at a time when ScotRail is failing to hit performance targets, passengers have every right to be angered at the government's failure to get a grip of our rail system.
"Mr Yousaf passed the buck to Network Rail this morning and then admitted he wasn't even a transport expert.
"There have been plenty of warnings about the cost over-runs at Network Rail. The least people expect is a Minister with the expertise necessary to get a grip."