It comprises two blocks: a cylindrical events hall, affixed to a cuboid containing a hotel and meeting rooms.
Dutch firm OMA claims have taken inspiration from Frank Lloyd Wright's New York Guggenheim for the building's design, which features smooth white concrete facades. These are perforated by bands of irregularly shaped windows.
Located on 33rd Street, the building lies at the centre of the Faena District Miami Beach development, which spans between the Atlantic Ocean and the Indian Creek waterway.
"Culture is at the core of Faena's vision, and has been the driving force for our collaboration in Miami Beach," said OMA partner Shohei Shigematsu.
"By curating their neighbourhood with programmatic diversity, Alan's sphere of influence will likely extend beyond this development to the rest of Miami Beach."
A wedge removed from the base of the cylindrical volume opens up a plaza on Collins Avenue.
Here, it joins the OMA-designed Faena Bazaar shopping centre within the restored 1930s Atlantic Beach Hotel and an automated car park. It also faces a new residential tower by Foster + Partners.
Inside, the drum-shaped volume is topped by a domed ceiling with a glazed oculus in its centre.
This 12-metre-high roof spans an auditorium, positioned above a bar and reception area, while an Assembly Hall spreads across the third floor of both blocks.
The building's opening, which coincides with the beginning of Art Basel Miami, will see the pop star Madonna take to the stage for a charity gig.
Another part of the same development is the renovation of the Saxony Hotel by Baz Luhrmann and Catherine Martin. Nearby hotels Casa Claridge and Versailles have also been overhauled by Faena.
The new cultural forum will become a sister institution to the arts centre in the Faena District Buenos Aires, Faena's first major development that spreads along a section of the waterfront in the Argentinian capital.
"We think Miami is the capital of Latin America at the moment," Shigematsu told Dezeen in an interview about the transformation of the city's skyline. "It's a gateway for Latin America to come into the United States."
OMA and its founder Rem Koolhaas comes in at number 12 on the Dezeen Hot List, our comprehensive guide to the most newsworthy and searched-for players in the design world in 2016.