Wagner chief Yevgeny Prigozhin, once a close Putin ally, said his troops had taken control of the military command center and bases in the southern city of Rostov-on-Don, the nerve centre of Russia's offensive in Ukraine, and vowed to topple Moscow's top military leaders.
Further north, on Wagner's possible route towards Moscow, the governor of Russia's Voronezh region said the armed forces had launched a "counter-terrorist operation" to suppress the revolt. A fuel depot on Voronezh city was on fire, he said.
The FSB security service accused Prigozhin of attempting to launch a "civil conflict" and urged Wagner fighters to detain him.
Responding to the challenge in a televised address, Putin accused Prighozin -- whose private army provided shock troops for Moscow's offensive in Ukraine -- of a "stab in the back" that posed a threat to Russia's very survival.
"Any internal turmoil is a deadly threat to our statehood and to us as a nation. This is a blow to Russia and to our people," Putin said.
"This battle, when the fate of our people is being decided, requires the unification of all forces."
"Extravagant ambitions and personal interests led to treason," Putin said, referring to Prigozhin, who built his powerbase as a catering contractor to the Kremlin and now runs a private military force.
"All those who consciously stood on the path of betrayal, who prepared an armed rebellion, stood on the path of blackmail and terrorist methods, will suffer inevitable punishment, before the law and before our people," Putin vowed.
The Russian president's speech came shortly after Prigozhin posted a message of his own, apparently filmed in Rostov-on-Don, accusing the Russian military leadership of betrayal and failure in the ongoing battle against Ukrainian forces.
"A huge amount of territory is lost. Soldiers have been killed, three, four times more than what it says in documents shown to the top," he said, accusing commanders of hiding the true scale of Russian losses in Ukraine from the Kremlin.
"Military sites in Rostov, including an aerodrome, are under control," he said, adding that warplanes taking part in the Ukraine offensive "are leaving as normal".
Inside Ukraine, emergency services said that three people were killed and nearly a dozen injured in Kyiv after what authorities said was an overnight barrage of 40 Russian cruise missiles and at least two attack drones.
- 'Civil conflict' -
After Putin's speech accusing him of treason, Prigozhin launched a second broadside.
"On treason of the motherland: the president is deeply wrong. We are patriots of our motherland," Prigozhin said. "Nobody plans to turn themselves in at the request of the president, the FSB or anyone else."
Russia's headquarters in Rostov-on-Don is a key logistical base for its offensive in Ukraine.
Watching events unfold in Russia as his own forces conduct a slow-moving counteroffensive, Ukraine's President Volodymyr Zelensky said the revolt showed Russia's was failing.
"Russia's weakness is obvious. Full-scale weakness," he said.
"And the longer Russia keeps its troops and mercenaries on our land, the more chaos, pain, and problems it will have for itself later. It is also obvious, that Ukraine is able to protect Europe from the spread of Russian evil and chaos."
News photographs showed armed men surrounding administrative buildings in Rostov and tanks deployed in the city centre. It was not clear who the armed men were.
The mayor of Moscow announced that "anti-terrorist" measures were being taken in the capital and authorities said security had been tightened in several regions.
Critical facilities were "under reinforced protection", TASS reported, citing a law enforcement source.
- Missile strikes -
Prosecutor General Igor Krasnov had informed Putin of "the initiation of a criminal case in connection with an attempt to organize an armed rebellion", Kremlin spokesman Peskov said.
While Prigozhin's outfit fought at the forefront of Russia's offensive in Ukraine, in recent months it has engaged in a bitter feud with Moscow's military leadership.
He has repeatedly blamed Defense Minister Sergei Shoigu and Valery Gerasimov, chief of the general staff, for his fighters' deaths.
The Russian defense ministry warned that Ukrainian troops were taking advantage of the infighting to ready an assault near the eastern hotspot of Bakhmut.
A prominent Russian general urged Prigozhin to call off efforts to remove the defense ministry leadership.
"I urge you to stop," Sergei Surovikin, commander of Russia's aerospace forces, said in a highly unusual video address.
Washington-based think tank the Institute for the Study of War said the Wagner chief's attempt to force a leadership change in the defence ministry "is unlikely to succeed" given that Surovikin had denounced his call for rebellion.
However, it said Wagner's apparent capture of Rostov-on-Don "would have significant impacts on Russia's war effort in Ukraine".
US President Joe Biden was briefed on the situation in Russia and Washington "will be consulting with allies and partners on these developments", National Security Council spokesman Adam Hodge said.
France and Germany said they were closely following events. Italy warned its citizens in Russia to take care and UK Prime Minister Rishi Sunak urged "all parties" to spare civilian life.
