The 41-year-old father of three and an opposition politician who holds Russian and British passports, spoke out against President Vladimir Putin for years and successfully lobbied Western governments to impose sanctions on Russia and individual Russians for purported human rights violations.
State prosecutors, who had requested a 25-year term, had accused him of treason, among other offences, and of discrediting the Russian military after spreading "knowingly false information" about its conduct in what Moscow calls its "special military operation" in Ukraine.
His sentence was the harshest handed down to a Kremlin critic since Putin came to power in 1999.
In a CNN interview broadcast hours before his arrest, Kara-Murza, whose family home is in Washington and who had returned to Moscow to campaign against the war, alleged that Russia was run by a "regime of murderers".
He had also used speeches in the United States and Europe to accuse Russia of bombing civilians in Ukraine, a charge Moscow has rejected.
After hearing he'd been ordered to spend the next quarter of a century in a maximum-security penal colony, Kara-Murza, who had calmly listened to proceedings inside a glass courtroom cage, declared "Russia will be free", an opposition slogan.
He also smiled and - according to one of his lawyers, Maria Eismont - said he regarded the harsh sentence as recognition of his work.
"When he heard he'd got 25 years he said: 'My self-esteem has gone up, I understand that I did everything right. It's the highest score I could have got for what I did, for what I believed in as a citizen and a patriot,'" she said.
His wife, Evgenia, echoed that sentiment on Twitter, likening his lengthy jail term to an “A+” for courage, consistency and honesty. "I am infinitely proud of you, my love, and I’m always by your side," she wrote.
Separately, she told a Washington Post event that the sentence showed how much the Russian authorities feared her husband.
In his final speech in court last week, Kara-Murza compared his trial, held behind closed doors, to Josef Stalin's show trials in the 1930s. He declined to ask the court to acquit him, saying he was proud of everything he had said and done.
Eismont, who said her client had not been allowed to speak to his children by phone for nearly a year, said Kara-Murza's team would appeal against Monday's verdict, which she said had been marred by legal violations.
The Kremlin, when asked about the verdict, said it did not comment on court decisions. A prominent state TV host said Kara-Murza had got what he deserved.
ENVOY SUMMONED
In London, Britain - which in 2020 imposed sanctions on the judge presiding over the case for alleged human rights violations - said it had summoned the Russian ambassador to protest over what it called a "politically-motivated" conviction.
Outside the Moscow court, British Ambassador Deborah Bronnert told reporters that Kara-Murza had been punished for bravely speaking out against Russia's war in Ukraine and demanded his release.
US Ambassador Lynne Tracy, speaking alongside her, said Kara-Murza's conviction was an attempt to silence dissent.
"Criminalisation of criticism of government action is a sign of weakness, not strength."
Russian Foreign Ministry spokeswoman Maria Zakharova criticised the Western diplomats' intervention, suggesting they might be called in to be reminded of what "diplomats should and shouldn't do."
Shortly after sending tens of thousands of troops into Ukraine in February last year, Russia introduced sweeping wartime censorship laws which have been used to silence dissenting voices.
"Discrediting" the army can currently be punished by up to five years in prison, while spreading deliberately false information about it can attract a 15-year jail sentence.
Casting the conflict in Ukraine as an existential struggle with the West, Russian pro-government politicians say unity across society is vital. They have described Russian citizens who question Moscow's actions in Ukraine as part of a pro-Western fifth column trying to undermine the military campaign.
Twice, in 2015 and 2017, Kara-Murza fell suddenly ill in what he said were poisonings by the Russian security services, on both occasions falling into a coma before eventually recovering.
Russian authorities denied involvement in those incidents. Kara-Murza's lawyers say that as a result, he suffers from a serious nerve disorder called polyneuropathy.
Eismont, his lawyer, said his legal team was concerned about his health after an examination by a civilian hospital at the end of March found his condition was worsening.
Jailed opposition politician Alexei Navalny, whose own health is under pressure, told a legal hearing that Kara's Murza's conviction was illegal and looked like punishment for him not dying after being poisoned.
Tatiana Stanovaya, founder of the R.Politik analysis firm, said Kara-Murza's lobbying for sanctions on Russia had long irritated the Kremlin and that his conviction - which leaned on a newly-expanded definition of treason - was a warning.
"This is a verdict aimed at sending a signal and probably not the last of its kind," she wrote on the Telegram messaging app.
"In future, the security services can be much less choosy and seize anyone if they are on Russian territory and a critic of the Putin regime. This is a warning to all anti-Putin activists - don't come back or we'll put you in jail, de facto for life."