Havelock House, the home of UTV, has gone on the market for £3.5m.
Listed by estate agents Savills, the property on the Ormeau Road will shut its doors for the last time in June after 60 years serving as a broadcasting studio.
Down the years it has welcomed stars from all over the globe, including Garth Brooks, Elton John and Sean Connery, and kickstarted the careers of broadcasters Eamonn Holmes and Gloria Hunniford.
Last year the commercial television broadcaster revealed that it would relocate to City Quays 2 in Belfast Harbour Estate where it will occupy almost 12,000sq ft of top floor space and nine floors of office space.
UTV's head of news and programmes Terry Brennan said the property listing is "another important milestone" in that office move.
"Havelock House has served us well for almost 60 years, but we are looking forward to moving to the eighth floor of City Quays 2," he said.
"As well as the breathtaking views, our new location will be home to a modern broadcasting centre, with a HD studio; the latest in editing technology; and corporate offices, with administration, finance and sales areas to accommodate all UTV staff."
UTV - which was taken over by ITV plc in a £100m deal two years ago - has been situated at Havelock House since the broadcaster went live in October 1959.
The first voice on air that day was Sir Laurence Olivier.
It has produced programmes including The Kelly Show, School Around The Corner, Lesser Spotted Ulster, Counterpoint and Farming Ulster.
It was also used by television film crews around the world to process and edit film footage of the Troubles.
The property, which sits on a 1.78-acre site and comes with almost 60,000sq ft of office and production space, has an illustrious history steeped in Belfast's heritage.
Before it was converted into a television studio it was the site of a hemstitching warehouse.
During the Second World War the building provided a billet for troops who were tasked with providing protection for the city's numerous bridges.
Ulster Television acquired the premises at a cost of £17,000 and in 1962 and again in 1992 it extended the building.
Simon McEvoy, divisional director at Savills Northern Ireland, said he expected a high level of interest in the sale from both local and international investors.
"There are a number of opportunities... including the development of residential or office accommodation," he said.
He added that the refurbishment of the existing structure was also an option.