For close to four decades, Hun Sen, the prime minister of Cambodia, maintained his grip on power by upholding a simple conceit: The country needed him, and, as such, he could never retire.

Not anymore.

On Tuesday, Mr. Hun Sen, 71, transferred the premiership to his son, Gen. Hun Manet, a 45-year-old graduate of the United States Military Academy at West Point and chief of the Cambodian Army. The move caps a generational shift so rare that three out of four Cambodians have only ever known Mr. Hun Sen as their leader.

“It’s a once-in-a-lifetime experience for many Cambodians to see political change,” said Chhengpor Aun, a visiting fellow at the International Institute for Strategic Studies specializing in Cambodian politics.

Mr. Hun Sen, one of the world’s longest-ruling prime ministers, has made it clear that he will not be leaving Cambodian politics completely. He remains the head of the leading Cambodian People’s Party and has said that he would remain in office as Senate president until 2033. In June, he said that even though he was stepping down, he would “still control politics” as the head of the C.P.P.

But the transition of power has significant implications for Cambodia’s future, Southeast Asia and for the United States and China, which are jockeying for influence in the region. One of the main questions surrounding Mr. Hun Manet is whether he may be open to cooperating more closely with the West as he leads a generational change that will bring the internationally educated children of current ministers into power for the first time.

Many Cambodian activists have warned that history is replete with the Western-educated children of autocrats — from Kim Jong-un of North Korea to Bashar al Assad of Syria — going on to rule more harshly than their fathers. The opposition does not expect Mr. Hun Manet to be any different.

In a speech to the National Assembly on Tuesday, Mr. Hun Manet said it was “necessary to continue leading the country peacefully and securely, and to maintain development and make reforms in all sectors.”

Mr. Hun Sen told reporters that it was “an ignorant statement” to suggest he would lead the country by proxy despite leaving his post and handing power to his son.

When Mr. Hun Sen became prime minister 38 years ago, the country was emerging from the destruction of the Khmer Rouge movement. He ushered in an era of strongman rule that has included the eradication of opposition parties and independent media. In July, the C.P.P. claimed it had clinched a “landslide victory” in elections that international observers said were stage-managed and unfair.

But in a region where political dynasties are common, few Cambodians appear to have a problem with Mr. Hun Manet taking over when his father’s rule has been largely marked by 30 years of rising economic growth and a period of uninterrupted stability.

As leader, Mr. Hun Sen embraced China, which he described as Cambodia’s “most trustworthy friend.” Beijing, Cambodia’s largest trading partner, supplied loans to finance airports, roads and other infrastructure projects.

In return, Mr. Hun Sen’s government repeatedly blocked criticism of China at meetings of the Association of Southeast Asian Nations, frustrating members, such as the Philippines and Vietnam, both locked in territorial disputes with Beijing over the South China Sea. In July, Cambodia broke ground on a naval base that the United States has warned could be an overseas outpost for the Chinese military. Both Phnom Penh and Beijing have denied the charge.

It has been clear for about a decade that Mr. Hun Sen would pass the baton to his eldest son. “This is our preparation for the long-term stability of our country,” Mr. Hun Sen said when he made the announcement on July 26.

He added that it was essential for a new, younger cabinet to “receive their duties early” and that his son was “not inheriting this role without a legitimate process.” Although Mr. Hun Manet has never held elected office, he participated in the recent election as a lawmaker candidate, making him eligible to be appointed prime minister, according to his father. (Mr. Hun Manet’s youngest brother, Hun Many, will be the minister of civil service.)

“This is a significant renunciation for me, but this renunciation ensures the happiness of our people,” Mr. Hun Sen said.

During the election, Mr. Hun Manet was often seen taking selfies and flashing finger hearts with voters. People who have interacted with him say he is down-to-earth and open to new ideas.

“At the very least he doesn’t expect me to kowtow,” said Ou Virak, the president of Future Forum, a think tank in Cambodia that focuses on public policy. He added that this was a dramatic departure from his interactions with officials in Mr. Hun Sen’s administration.

Still, analysts say it is unlikely that Mr. Hun Manet will veer too far from his father’s policies. In January, he called on opposition parties to stop engaging in campaigns with “insults and smears,” which some saw as a veiled threat. Few Cambodians expect him to dismantle the patronage networks that his father established or to tackle the corruption, deforestation and land grabs that have become endemic in this nation of 16.6 million.

While he may seek to recalibrate ties with the West in an effort to gain leverage in an era of great superpower rivalry, he won’t abandon China, said Kalyan Ky, the former president of the Cambodia-Australia-New Zealand Exchange Mission and an acquaintance of the new prime minister.

Mr. Hun Manet “was really receptive to the idea of connecting with the West but also keeping China happy at the same time,” added Ms. Ky.

When asked in June whether his son would govern differently, Mr. Hun Sen said: “In what way? Any such divergence means disrupting peace and undoing the achievements of the older generation.”

Like his father, Mr. Hun Manet is also likely to focus on economic growth. Tourism has not fully recovered since the coronavirus pandemic, and Cambodia’s economy is heavily dependent on China, where a flailing property market has signaled a potential economic crisis.

Yet any change in a country with a ruler who boasted of being in power for “14,099 days” is likely to carry some hope.

Mr. Hun Manet was the first Cambodian to graduate from West Point in 1999. Later, he completed a master’s from New York University and a doctorate from the University of Bristol in England, both in economics.

He rose quickly through the ranks of Cambodia’s military and is now a four-star general and deputy commander in chief of the Royal Cambodian Armed Forces. In 2020, he became head of the C.P.P.’s youth wing.

“The parents said that he was the brightest among them all,” said Julie Mehta, who co-wrote a biography on Mr. Hun Sen with her husband, Harish Mehta.

Mr. Hun Manet “drew important lessons from his exposure to the American way of life, with its focus on individual rights and responsibilities,” said Mr. Mehta, who, along with his wife, interviewed Mr. Hun Sen, Bun Rany, Mr. Hun Sen’s wife, and Mr. Hun Manet for the book.

When he was in his 20s, Mr. Hun Manet told the Mehtas that he liked that in the United States, “people can have the freedom and opportunity to do anything they want, provided their actions do not interfere with others, and do not break any laws.”

“Such freedom creates an environment for promoting innovation, creativity,” he said.

He added that he was frustrated by the negative reports of Cambodia, “largely by Western media,” and that the West focused too much on “problems and less on positive developments taking place in Cambodia.”

As an untested leader, Mr. Hun Manet has yet to prove he can fend off the challenges posed by political rivals. But his father has already assured Cambodians that they can rest easy: If his son faces a threat to his life or “fails to meet expectations,” Mr. Hun Sen said, he would return as prime minister.

Sun Narin contributed reporting.