Victoria Arnold's Desk Union venture has signed a contract with the bank under which it will create a community work space in the lender's flagship branch at 36 St Andrew Square.
The new facility on the first floor of the building will provide 24 work spaces and a meeting room, which will be available for hire by the hour.
Ms Arnold said: "The way we work is changing. We are no longer restricted to set hours or based in office cubicles. Businesses crave touchdown work space, where workers can meet, connect and collaborate with like-minded co-workers."
Desk Union is talking to RBS about opening similar centres in other branches.
Chris Wilson, managing director of branch and private banking, Royal Bank of Scotland, said: "I am delighted to be able to support Desk Union.
"Royal Bank of Scotland is playing the leading role in Scotland in supporting entrepreneurs and this is yet another example of RBS' commitment to getting the economy moving. The money made from this project will be re-invested back into creating similar work spaces around the country."
A graduate of the Entrepreneurial Spark programme for young businesses, Ms Arnold founded Desk Union in 2012 to link companies that had spare space with workers who needed accommodation.
The historic banking hall on the ground floor of 36 St Andrew Square will retain its current function.