The funding is part of package agreed by Deputy First Minister John Swinney and Dundee City Council on 26 February.
The Scottish Futures Trust's (SFT) Growth Accelerator model (GA) is designed to stimulate growth, create jobs and support businesses via a combination of public and private sector investment in local infrastructure and public spaces.
The £63.8m fund will be targeted towards improvements to Dundee railway station concourse, development of the V&A Museum of Design and ensuring the Waterfront contains 'world class' digital infrastructure.
In addition, 4,500 sq m of Grade A office space will also be developed alongside improvements to civic spaces.
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Mr Swinney said the investment underlines the government's commitment to Dundee.
"The nature of this funding model enables investment to be unlocked now that will support development in the area and longer term economic growth," he said.
"Today's package includes £13 million for the Dundee Railway Stations concourse in addition to the £4.3 million wider station development and £3 million to establish a future-proofed digital corridor to assist the city's world renowned games industry and provide a competitive digital solution to support economic development.
"We are also providing up to £20 million to further support the development of the V&A and over £25 million to redevelop the two civic spaces at Discovery Plaza and Waterfront Place.
"Our existing infrastructure investment programme is already working to improve connectivity and stimulate economic growth."
Council Leader Ken Guild added: "The V&A is already creating jobs and injecting money into Dundee's economy during the construction phase and generating a halo effect by attracting significant private investment.
"In the past two weeks alone we have had more than £70m of such investment announced in the wider Waterfront regeneration project and Dundee Port.
"Right now there is an unprecedented level of investor interest in Dundee and this announcement will help to reinforce that."
[Pictured: Design for the new Dundee Railway Station]
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