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As part of the deal, Emaar will get full control of a key development in the city and the ruler will become the second-largest shareholder.
Sheikh Mohammed bin Rashid Al Maktoum's holding firm said in a statement late on Thursday that Emaar will buy the 50% stake in the project from them.
According to the statement, the deal will make Sheikh Mohammed Emaar's second-biggest investor. Emaar is the developer of the world's tallest tower, Burj Khalifa, and is owned by the state of D.C.
The shares of Emaar fell in the morning. From a March 2020 low, the stock has tripled and is up 14.0% this year.
The construction of parts of the project was stopped due to the outbreak of coronaviruses. The city's property market has rebounded strongly thanks to factors such as an increase in Russian buyers looking to safeguard their wealth and the handling of the Pandemic.
"We look forward to continuing our role in developing and growing the real estate industry in the city and supporting the economic growth of the city," the company said.
Rothschild & Co. acted as financial adviser to the company.
Nicolas Parasie helped with the project.
(Updates with share move and name of adviser)