The court accuses Mr Putin and his children’s rights commissioner, Maria Alekseyevna Lvova-Belova, of “unlawful deportation” of children “from occupied areas of Ukraine to the Russian Federation”.
It means the court’s 123 member states must detain Mr Putin and him over for trial if he sets foot on their territory.
He becomes only the third serving president in history to be issued a warrant, after Sudan’s Omar al-Bashir and Libya’s Muammar Gaddafi.
It is one of the most ambitious cases that the ICC has undertaken, and the symbolism of the first warrant issued over Russia’s invasion is marked by going right to the top of the Kremlin.
Ukrainian President Volodymyr Zelensky called it a “historic decision, from which historic responsibility will begin”.
But Kremlin spokesman Dmitry Peskov said Russia does not recognise the ICC and considers its decisions “legally void”. Ex-president Dmitry Medvedev described the warrants as “toilet paper”.
ICC chief prosecutor, Karim Khan, said that “many of these children, we allege, have since been given up for adoption in the Russian Federation” and that a Russian law change has made it easier for the children to be adopted by families.
“We must ensure that those responsible for alleged crimes are held accountable and that children are returned to their families and communities... we cannot allow children to be treated as if they are the spoils of war,” Mr Khan said.
Ms Lvova-Belova said last month she had “adopted” a child from the Ukrainian city of Mariupol, now under Russian control.
“It’s great that the international community has appreciated this work to help the children of our country: that we don’t leave them in war zones, that we take them out, that we create good conditions for them, that we surround them with loving, caring people,” she said, according to RIA Novosti.
Mr Khan said multiple, interconnected investigations are continuing. “Ukraine is a crime scene that encompasses a complex and broad range of alleged international crimes. We will not hesitate to submit further applications for warrants of arrest when the evidence requires us to do so.”
Britain’s foreign secretary, James Cleverly, welcomed the steps by the ICC “to hold those at the top of the Russian regime” to account. “Work must continue to investigate the atrocities committed,” he tweeted.
Andriy Yermak, chief of Ukraine’s presidential staff, said the warrant was “only the beginning”. Ukraine has cooperated closely with the ICC and was currently investigating over 16,000 cases of forced children deportation to Russia, he said. It has managed to secure the return of 308 children so far.
Mr Khan opened his investigation into possible war crimes, crimes against humanity and genocide in Ukraine a year ago. He highlighted during four visits that he was looking at alleged crimes against children and the targeting of civilian infrastructure by Moscow’s repeated missile assaults.
A recent US-backed report by researchers at Yale University said Russia has held at least 6,000 Ukrainian children at sites in Russian-held Crimea. The report identified at least 43 camps and other facilities where Ukrainian children have been held that were part of a “large-scale systematic network” operated by Moscow.
Although the issue of a warrant is deeply embarrassing for Mr Putin, it is unlikely he will see the inside of a courtroom. Russia signed the Rome Statute in 2000, but never ratified it to become a member of the ICC, and finally withdrew its signature in 2016. The court relies on its 123 member states to enforce arrest warrants. The court's president, Piotr Hofmanski, said in a video statement: “The ICC is doing its part of work as a court of law. The judges issued arrest warrants. The execution depends on international cooperation.”
The ICC has the power to charge political leaders with “waging aggressive war” but given that Russia is not a signatory, that avenue was closed off, particularly as Moscow would also use its UN Security Council veto to limit further powers. However, it could leave Mr Putin marooned in his own nation.
Stephen Rapp, US ambassador-at-large for war crimes issues under former president Barack Obama, said: “This makes Putin a pariah. If he travels, he risks arrest. This never goes away. Russia cannot gain relief from sanctions without compliance with the warrants.”
Mr Peskov said Russia found the questions raised by the ICC “outrageous and unacceptable”. Asked if Mr Putin now feared travelling to countries that recognised the ICC, Mr Peskov said: “I have nothing to add on this subject. That’s all we want to say.”
The ICC warrant came a day after a UN-backed investigative body accused Russia of committing wide-ranging war crimes in Ukraine, including wilful killings and torture, in some cases making children watch loved ones being raped and detaining others alongside dead bodies.