He said such cities as London, Sydney, Paris, Rome and Barcelona will continue to grow quickly as they consolidate their power as hubs of knowledge-based industries like technology, finance and media.
The best cities will also be boosted by a boom in lodging.
"The hotel business will be a huge beneficiary of rising global affluence and tourism, especially from China," said Gray, who is also the chairman of global hotel business Hilton Worldwide.
(Read more: Future growth in China? The answer Is megacities)
The ever-expanding metropolis
Generally, those cities will widen in value in comparison to nearby rural and suburban areas. The U.S. will be no exception in 2039, according to Gray.
"In the U.S., the value of real estate in the great cities will continue to grow much faster than in the rest of the country. There will be even wider spreads between the cost of housing in, say, New York City versus New York state," he said. "This next 25 years I believe urban America will grow faster than suburban America."
Grey said gentrification would continue to expand the reach of large cities like San Francisco (via Oakland), London (moving north); and New York (via Queens and The Bronx).
The city trend also applies to frontier and emerging markets.
"Rapidly urbanizing cities in the frontier markets of Africa and Southeast Asia will benefit from favorable demographics, cheap labor and a rising middle class," said LaSalle's Gordon.
Gordon said the cities most likely to benefit include Accra in Ghana, Lagos in Nigeria, Nairobi in Kenya, Johannesburg in South Africa, Jakarta in Indonesia, and Phnom Penh in Cambodia.
LaSalle isn't the only one bullish on the future of real estate in Africa.
"Emerging markets in Africa will provide extraordinary returns, with much higher risk over longer periods of time," said Tom Barrack, founder of $31 billion private equity real estate company Colony Capital.
"Since there is no liquidity and very little transparency in their markets, correctly formulated investments will provide extraordinary returns as Africa redefines itself in oil and gas, agriculture and minerals," Barrack added.
(Read more: Countries with the most multimillionaires)
Those views on developing markets echo a recent report by McKinsey & Co. on the coming shift of large companies into now-less developed countries.
The global consulting firm estimates that more than 45 percent of the Fortune Global 500 could be based in emerging regions by just 2025, up from 5 percent in 1990 and 17 percent in 2010. There will also be three times as many large company headquarters in emerging regions as in 2010 by 2025.
A more public marketplace
Real estate in 2039 will be marked by more public investment, not just regional shifts.
"The desire to own real estate will be high. A greater and greater percentage of properties will end up in the public markets—a lot more than where we sit today," said Gray.
He projects that real estate investment trusts, which trade like stocks, will increasingly be used by retail investors. And real estate debt will be held more broadly; it won't just be banks and big institutions anymore, according to Gray.
He noted that the bond-like nature of real estate investing—relatively steady returns with the chance at appreciation in value—will appeal to aging investors looking for more stable assets to park money in.