Russia's loss of the bastion of Lyman, which puts western parts of Luhansk region under threat, touched a nerve for Ramzan Kadyrov, the leader of the southern Russian republic of Chechnya.
Kadyrov, who has been close to Putin since his father and former president of Chechnya, Akhmad, was killed in a 2004 bomb attack in Grozny that also killed a Reuters photographer, suggested that Russia should consider using a small tactical nuclear weapon in Ukraine in response to the loss.
The nuclear warning caught the headlines, but his public scorn for Russia's top generals may have been just as significant in a Russia where public criticism of the war effort from within the top echelons of the elite has been taboo.
"Nepotism in the army will lead to no good," Kadyrov said, adding that the commander of Russian forces in the area should be stripped of his medals and sent to the front line with a gun to wash away his shame with blood.
Such public contempt for the generals running Russia's war is significant because it indicates the level of frustration within Putin's elite over the conduct of the war while also piercing the Kremlin's carefully controlled narrative.
Kadyrov, who supports the war and has sent many of his own Chechen units to fight, said his criticism was the bitter truth about a Russian fighting force which he said allowed talentless mediocrities to let down the country.
The defence ministry did not respond to a request for comment. Russian officials say the history of Russian warfare shows that fighting often begins badly until the military can be properly organised. Writing off Russia, they say, is a poor bet.
Asked about Kadyrov's remarks on using a nuclear weapon, Kremlin spokesman Dmitry Peskov said on Monday: "This is a very emotional moment."
"The heads of regions have the right to express their point of view," Peskov told reporters. "Even at difficult moments, emotions should still be excluded from any assessments."
More than seven months into a war that has killed tens of thousands and triggered the biggest confrontation with the West since the 1962 Cuban Missile Crisis, even Russia's most basic war aims are far from achieved.
The vast army of a former superpower has been humbled on the field of battle by a much smaller Ukrainian force backed up with weapons, intelligence and advice from Western powers led by the United States.
In a fresh setback for Moscow on Monday, a Russian-installed official confirmed Ukrainian advances along the west bank of the Dnipro River in Kherson region in southern Ukraine, one of four regions Putin claimed last week to have annexed.
Putin says Russia is now locked into an existential battle with the West, which he accuses of seeking to destroy his country. Russia, he says, will prevail in Ukraine - and has warned that he is only just starting to get serious.
On Russian state television, humility appeared to be seeping into the usual jingoistic rhetoric.
"I'd really like us to attack Kyiv and take it tomorrow, but I'm aware that the partial mobilisation will take time," presenter Vladimir Solovyov said on Rossiya 1 state television.
"For a certain period of time, things won't be easy for us. We shouldn't be expecting good news right now."
The Chechen leader said he had raised the possibility of a defeat at Lyman two weeks ago with Valery Gerasimov, chief of Russia's general staff, but that Gerasimov had dismissed the idea.
Gerasimov, 67, is the third most powerful man in the Russian military after Putin and Defence Minister Sergei Shoigu. Shoigu landed Gerasimov the top military job just a few days after he was appointed defence minister in 2012.
"I do not know what the defence ministry reports to the supreme commander-in-chief (Putin), but in my personal opinion, more drastic measures should be taken," said Kadyrov, who shed tears for the fallen at a ceremony in the Kremlin last week at which Russia formally annexed the four Ukrainian regions.
In an indication of his influence, Kadyrov's other posts showed him meeting two of the Kremlin's most powerful men: Putin's chief of staff, Anton Vaino, and Sergei Kiriyenko, the powerful first deputy chief of staff.
Asked about Kadyrov's remarks, the powerful founder of the Wagner Group of mercenaries, Yevgeny Prigozhin, congratulated the Chechen leader.
"Ramzan - you rock man!" Prigozhin, known as Putin's chef due to his company's Kremlin catering contracts, said in a statement. "All these bastards should be sent barefoot to the front with automatic guns."
When asked if his words should be considered criticism of the defence ministry, Prigozhin doused his reply with irony: "God forbid".
"These statements are not criticism, but merely a manifestation of love and support," said Prigozhin, who the United States says runs a mercenary army that has dabbled in conflicts in Mali, the Central African Republic, Libya and Syria.
"I, and Ramzan Akhmatovich even more so, are the most cultured of people," Prigozhin said, using Kadyrov's patronymic as a sign of respect.
(Reporting by Guy Faulconbridge; Editing by Gareth Jones)
By Guy Faulconbridge and Felix Light