The test, alongside a nuclear drill last week, sends a message that Russia, in Putin's words, will never bow to pressure from the West over the war in Ukraine as US President Donald Trump takes a tougher stance against Moscow to push for a ceasefire.
Russia's top general, Valery Gerasimov, chief of the general staff of Russia's armed forces, told Putin the missile travelled 14,000km and was in the air for about 15 hours when it was tested on October 21.
Russia says the 9M730 Burevestnik (Storm Petrel) - dubbed the SSC-X-9 Skyfall by NATO - is "invincible" to current and future missile defences, with an almost unlimited range and unpredictable flight path.
"It is a unique ware which nobody else in the world has," Putin, dressed in camouflage fatigues at a command point meeting with generals overseeing the war in Ukraine, said in remarks released by the Kremlin on Sunday.
Since first announcing the 9M730 Burevestnik in 2018, Putin has cast the weapon as a response to moves by the US to build a missile defence shield after Washington in 2001 unilaterally withdrew from the 1972 Anti-Ballistic Missile Treaty, and to enlarge the NATO military alliance.
Putin said on Sunday he had once been told by some Russian specialists that the weapon was unlikely to ever be possible, but now, he said, its "crucial testing" had been concluded.
He told Gerasimov Russia needed to understand how to classify the weapon and prepare infrastructure for deploying the Burevestnik.
But the timing of the missile test - and its announcement by Putin in fatigues at a meeting at a command point with generals in charge of the Ukraine war - sends a signal to the West and to Trump in particular.
The White House did not immediately respond to a request for comment on the missile.
For Trump, who has cast Russia as a "paper tiger" for failing to swiftly subdue Ukraine, the message is that Russia remains a global military competitor, especially on nuclear weapons, and that Moscow's overtures on nuclear arms control should be acted on.
Putin's message for the broader West, after the US moved to provide Ukraine with intelligence on long-range energy infrastructure targets in Russia, is that Moscow can strike back if it wants to.
After The Wall Street Journal reported that the Trump administration has lifted a key restriction on Ukraine's use of some long-range missiles provided by Western allies, Putin said on Thursday that if Russia were attacked, the response would be "very serious, if not overwhelming".
Kremlin spokesman Dmitry Peskov repeated that message to Russian state TV in remarks published on Sunday.
Gerasimov said the missile had flown on nuclear power and the test had been different because it flew for such a long distance, although the range was essentially unlimited.
He said it could defeat any anti-missile defences.
Putin on Wednesday oversaw a test of Russia's strategic nuclear forces on land, sea and air to rehearse their readiness and command structure.
Gerasimov said that training launches of Yars and Sineva intercontinental ballistic missiles had been completed along with two Kh-102 air-launched cruise missiles.
"The so-called modernity of our nuclear deterrent forces is at the highest level," Putin said, higher than any other nuclear power.
In Ukraine, Gerasimov said Russian forces had encircled large numbers of Ukrainian soldiers around Pokrovsk in the Donetsk region, and were advancing in Kharkiv, Dnipropetrovsk and Zaporizhzhia regions.
