For years, Ilya Remeslo was a reliable pro-Kremlin operator, going after critics of the regime and smearing independent journalists, bloggers and opposition politicians.

Then the 42-year-old lawyer abruptly turned on the country’s most powerful man. Late on Tuesday, Remeslo posted a manifesto to his 90,000 Telegram followers titled: “Five reasons why I stopped supporting Vladimir Putin.”

In it, he accused the “illegitimate” Russian president of waging a “failing war” in Ukraine that had caused millions of casualties and wrecked the economy, and argued that Putin’s more than two decades in power illustrated how “absolute power corrupts”, calling on him to step aside.

The post sent shock waves through Russia’s online sphere, fuelling confusion over how such a loyalist could reverse course so abruptly – and whether the shift was genuine.

Doubling down on his earlier remarks, he told the Guardian on Wednesday from his flat in St Petersburg: “Vladimir Putin should resign and be put on trial as a war criminal. His personalised, corrupt system is doomed to collapse, as we’re seeing now with the war in Ukraine and elsewhere.

“The army isn’t advancing in Ukraine, and the war is going nowhere. There are massive losses. We are fighting over tiny territories that will ultimately give Russia nothing.”

He went on to criticise Putin’s authoritarian rule, the state of the economy and Moscow’s recent push to shut down internet access. “This man [Putin] has destroyed everything he could lay his hands on. The country is literally falling apart,” Remeslo said.

While members of Russia’s pro-war community, known as “Z-bloggers”, have at times criticised the country’s military leadership, very few have openly challenged Putin or the broader rationale behind the invasion.

Remeslo’s wide-ranging tirade, therefore, marked a rare breach of longstanding taboos, said Ivan Philippov, a researcher of the pro-war movement. “This really is unprecedented,” he said. “I am struggling to make sense of it.”

Remeslo, a former member of Russia’s public chamber, a Kremlin-controlled advisory body, has long been known as a regime henchman who used his legal background to target and denounce critics of the authorities both in court and online. Much of his work centred on campaigns targeting the late opposition leader Alexei Navalny, appearing in courtrooms across the country to testify against him.

Remeslo’s 180-degree turn provoked immediate speculation. Some initially suggested his account could have been hacked – a theory quickly dismissed after Remeslo published a video repeating his claims. Others argued it could be a form of Kremlin political dark arts – a staged provocation to identify those who might support him.

Remeslo may have been having a “mental breakdown”, Philippov said.

Remeslo claimed that “none of this is staged. I am just speaking the truth” and denied that he had been directed by anyone, saying: “People really overestimate the current administration. They wouldn’t come up with such a plan.”

Asked why he had chosen to speak out now, Remeslo said the decision had developed gradually until he felt he could no longer remain silent. “Putin is no longer ‘one of us’. He is a person whose interests are completely alien to both Russia and me personally. I’ve come to the conclusion that it is both possible and necessary to criticise him, because otherwise none of this will stop and nothing good will come of it,” he said, adding that many other members in the community “thought the same way”.

Remeslo said he had been receiving frantic calls throughout the morning from contacts in the security services, urging him to take down the posts, which he said suggested the system was panicking.

The Russian opposition appeared puzzled on Wednesday. Leonid Volkov, a close ally of Navalny and one of Remeslo’s long-time targets, said he initially suspected the episode was staged, but later changed his mind, saying the remarks went far beyond anything the Kremlin would sanction or orchestrate.

“He wrote and said things that simply cannot be said. People are jailed for far less … This opens a very dangerous Pandora’s box. It crosses every red line,” Volkov said.

Still, “it is hard to believe this was an act of personal courage or initiative”, Volkov added.

Remeslo’s outburst comes at a politically sensitive moment for Moscow, which has recently faced rare criticism even from its staunchest supporters over widespread mobile internet blackouts and disruptions to Telegram. Recent polling also suggests growing fatigue with the war, with a record number of Russians saying they would prefer it to end as economic pressures mount.

Nonetheless, western intelligence assessments and experts generally believe Putin’s system of power is resilient, marked by elite cohesion and tight control over society.

Remeslo said he was under no illusion that he could face prosecution for his remarks. Russian authorities have previously dealt ruthlessly with internal challenges, even among prominent nationalists. They handed a lengthy prison sentence to Igor Girkin, a prominent former separatist commander and outspoken critic of Putin, and purged his allies. Moscow is also believed to have been behind the death of Yevgeny Prigozhin, the mercenary leader who launched a short-lived mutiny against the authorities and later died when his plane crashed in murky circumstances

“I am ready for any trial against me,” Remeslo said. “The time has come to somehow break this vicious cycle and speak out. I bear a certain responsibility as someone who, for a long time, supported this regime and helped it survive.”