The red, white and blue colour scheme, which includes the Saltire, adorns the electric locomotive which hauls the daily 5:40am express from Edinburgh to London King’s Cross.
It is the fastest Scotland-London train, taking exactly four hours.
The new livery comes as the rebranding of the east coast train fleet nears completion after VTEC, which is 90 per cent Stagecoach-controlled, took over the franchise in March.
Flying Scotsman became the unofficial name of the Special Scotch Express train ten years after it was launched in 1862, with the name made official in 1924.
The train was later hauled by the Flying Scotsman steam locomotive from 1928.
Ms Sturgeon, speaking at Waverley Station in Edinburgh, said: “For over 150 years the Flying Scotsman service has connected Edinburgh and London by the historic East Coast rail route. “It is wonderful to see the name of the Flying Scotsman train kept alive on the route with a new, contemporary design.
VTEC managing director David Horne said: “We are thrilled to continue the legendary name of the Flying Scotsman.
“Flying Scotsman trains brought style to the railways for many years. Our new train is a design twist on the legendary Flying Scotsman, recreating the glamour of rail travel for the 21st century, using our distinctive Virgin brand and style.”
VTEC also announced a £16 million deal for the engine refurbishment of its separate 35-strong diesel “High Speed Train” fleet, which run between Aberdeen, Inverness and London.
The work, by engine manufacturer MTU, is the latest of a series of engine overhauls on the trains, which date back to the 1970s.
It will be done at the Craigentinny depot in Edinburgh over the next two years.
The trains will continue running until replaced by Hitachi Super Express trains in 2018.
However, ScotRail is due to introduce other versions of the trains, currently running on Great Western Railway, on inter-city routes the same year.