Putin embraced turmoil, and now it is rattling his leadership.

President Vladimir V. Putin of Russia always seemed to thrive on chaos. Now it threatens to consume him.

For the past few months, as the mercenary chieftain Yevgeny V. Prigozhin escalated his feud with the Russian military, Mr. Putin did not publicly reveal any discomfort with his diatribes. The silence fostered the kind of political ambiguity that has long been a trademark of Mr. Putin’s rule: a management style in which he appeared comfortable with conflicts among the elite because they kept potential rivals in check, while underscoring that ultimate authority always rested with the president himself.

Now that approach has backfired. On Saturday Mr. Prigozhin’s forces seized control of key military facilities in the southwestern city of Rostov-on-Don and threatened to march to Moscow, creating the most dramatic challenge to Mr. Putin’s rule since he was named Russia’s acting president on Dec. 31, 1999.

Mr. Putin’s tolerance of Mr. Prigozhin’s outbursts this year may have served his political purposes, but it prompted officials stunned by Mr. Prigozhin’s verbal attacks on Russia’s top brass to conclude that he enjoyed the president’s tacit support, analysts said. It also further emboldened Mr. Prigozhin.

“They were trying to decipher Putin’s behavior, because Putin was silent,” said Tatiana Stanovaya, a senior fellow at the Carnegie Russia Eurasia Center, referring to senior officials in the Kremlin and in the security services.

The confusion over Mr. Putin’s personal views only came to an end Saturday morning, when the president delivered a five-minute address to the nation describing Mr. Prigozhin — without naming him — as a traitor and vowing to quell the uprising the paramilitary leader had started. But the damage had already been done.

There was no sign that Mr. Putin’s hold on power was about to crumble. Other powerful men at the nodes of Mr. Putin’s informal power structure — like Ramzan Kadyrov, the strongman leader of the southern Russian region of Chechnya, who controls his own paramilitary force — publicly voiced their support for the president on Saturday.

Still, the events were a striking consequence of the informal power structure that Mr. Putin built up in his 23 years at Russia’s helm. For more than two decades, the system helped Mr. Putin secure his unrivaled authority, ensuring that he personally held the keys to wealth and influence in modern Russia.

People who know Mr. Putin say that the president has always been comfortable with that personalized system, because it allowed him to entrust key tasks to a trusted inner circle while preventing the rise of rival cliques that could undermine him. And it ensured that the institutions of the state — from the courts to Parliament to the news media to the multiple security services — remained mere instruments in internecine power plays mediated by Mr. Putin, rather than sources of influence in their own right.

One Russian business tycoon, reflecting on Mr. Prigozhin’s rise while speaking on the condition of anonymity, said that Mr. Putin’s approach to his rule was always “divide and conquer.” As another put it, referring to Russia’s rival law enforcement authorities: “You never know who will arrest you.”

A judo sparring partner from Mr. Putin’s youth became a construction billionaire and built Mr. Putin’s landmark bridge to Crimea. Buddies from Mr. Putin’s K.G.B. days now oversee Russia’s military industrial complex and its oil sector. A friend from 1990s St. Petersburg is entrusted with control of Russia’s most important private media assets and of the bank said to be at the nexus of Mr. Putin’s own financial dealings.

And then there was Mr. Prigozhin, who met Mr. Putin more than 20 years ago as a St. Petersburg restaurateur. He parlayed those personal ties into lucrative government contracts and styled himself as a ruthless, multipurpose problem solver on the Kremlin’s behalf.

In 2016, as the Kremlin sought to swing the American presidential election to Donald J. Trump, Mr. Prigozhin jumped into the fray with an internet “troll factory,” waging “information warfare against the United States.” As Russia worked to expand its reach in Syria and Africa, Mr. Prigozhin deployed his growing Wagner mercenary force to those regions — allowing the Kremlin to project power while minimizing Russian military boots on the ground.

In Ukraine, as Mr. Prigozhin tells it, Wagner troops were only called in after Mr. Putin’s initial invasion plan failed. For much of the war’s first year, Mr. Prigozhin appeared above the law, as he toured Russian prisons to recruit thousands of convicts to bolster his force.

By early this year, the Kremlin appeared to be taking some steps to limit Mr. Prigozhin’s rise. Television commentators were directed to avoid mention of him on air, and he lost his ability to recruit convicts.

But Mr. Putin seemed to vacillate on his own support for Mr. Prigozhin. In May, he congratulated Wagner mercenaries for their role in the capture of the Ukrainian city of Bakhmut, in a statement posted on the Kremlin’s website. Weeks later, he backed the Defense Ministry’s push for mercenaries to sign service contracts with the Russian military by July 1, a demand that infuriated Mr. Prigozhin.

Now, as Mr. Putin scrambles to put down a rebellion that he warned on Saturday could lead to “anarchy and fratricide,” Mr. Prigozhin looms as the Russian president’s own creation.

Mr. Prigozhin “had no real independent power base except the favor of the president,” Mark Galeotti, an expert on the Russian military and security services, said. “However this goes, it undermines Putin’s credibility and legitimacy.”

Neil MacFarquhar contributed reporting.