Moscow has in recent years touted the development of weapons that it hopes will give it the edge in any arms race with the United States at a time of growing tensions with the West.
Hypersonics can travel more than five times the speed of sound and manoeuvre in mid-flight, making them much harder to track and intercept than traditional projectiles.
The military said on Thursday it had fired the Zircon missile from the Admiral Gorshkov warship and hit a test target in Russia's Arctic waters.
"The shot was conducted on a sea target in the waters of the White Sea," Russia's defence ministry said in a statement carried by news agencies.
It added that the missile eliminated its target with a "direct hit".
The Zircon had already undergone several tests in recent years, including another launch from the Admiral Gorshkov and from a submerged submarine.
Putin used his state of the nation address in 2018 to reveal new hypersonic weapons, including the Zircon, saying it could hit targets at sea and on land with a range of 1,000 kilometres (620 miles).
The Zircon looks set to join Avangard hypersonic glide vehicles that were put into service in 2019 and the air-launched Kinzhal (Dagger) missiles in Russia's arsenal.
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