The current owner of Grade I listed mansion Marlborough House, in partnership with Oakley Property, has made all 9,200sq ft of the Old Steine site available on a rental basis.
Marlborough House was built in the 1760s for Samuel Shergold and later sold to the Duke of Marlborough.
Architect Robert Adam remodelled and extended it into its current neoclassical style.
From the late 1800s it was used by the Board of Schools and then as offices for Brighton & Hove Council before being sold in 1999.
It was the tourist information office until the creation of the unitary authority of Brighton & Hove and has been used as offices.
Commercial director at Oakley Property Steven Harvey said: “To see a building such as Marlborough House, which holds so much historical significance, come to market is a fantastic moment for the city.
“This really is a spectacular building and it’s brilliant to see that it will be once again used and appreciated by local residents and businesses.”
The property, which is available for a guide rent of £200,000 per annum exclusive, is arranged over lower ground floor and three upper floors and provides a variety of different-sized rooms on each level.
Marlborough House also has the potential to be considered for Class E use, which includes retail, restaurant, offices, financial services, gyms, medical and nursery uses.