Mr Hun Manet, who succeeded his father Hun Sen in August, hailed the Siem Reap Angkor International Airport as "modern" as he cut a ribbon to officially open it.
He said it was the first Cambodian air facility developed under Beijing’s Belt and Road global investment project, and the US$1.1 billion hub would stimulate tourism.
"It is another new historic event for the air transportation sector of Cambodia," he said.
"Our duty is to make this airport work," he said, "and to make this airport lift the standard of living of the people, to push the Cambodian economy."
The country once had one of the world’s fastest-growing economies – averaging an annual growth rate above 7% for two decades before the Covid-19 pandemic.
The new airport, with a 3,600 m runway, is located about 40 km from Cambodia’s famed Angkor temples park in Siem Reap, the country’s main tourist destination.
The city’s old airport was located just 5 km from the Unesco world heritage site.
Conservationists and officials have long voiced concerns that vibrations from frequent flights there were damaging the foundations of the centuries-old temples.
Officials said the new airport poses no threat to the ancient ruins. It will be given to Cambodia in 2073 after 50 years of operations under a Build-Operate-Transfer programme between the two countries.
Another huge airport is also under construction outside the capital Phnom Penh, costing US$1.5 billion and expected to open in 2025.
Tourism is hugely important to the country’s economy, but visitors nosedived to below 200,000 in 2021 from roughly 6.6 million before the Covid-19 pandemic.
Cambodia has received 3.7 million foreign tourists so far in 2023.