Defence Minister Sergei Shoigu informed his leader that the first missile unit equipped with the Avangard hypersonic glide vehicle entered combat duty, the Defence Ministry said.
"I congratulate you on this landmark event for the military and the entire nation," Mr Shoigu said later during a conference call.
The Strategic Missile Forces chief, General Sergei Karakayev, said during the call that the Avangard was put on duty with a unit in the Orenburg region in the southern Urals Mountains.
Putin unveiled the Avangard among other prospective weapons systems in his state-of-the-nation address in March 2018, noting that its ability to make sharp manoeuvre on its way to a target will render missile defence useless.
The Russian leader described the Avangard's creation as a technological breakthrough comparable to the 1957 Soviet launch of the first satellite.
The Russian leader noted that Avangard is designed using new composite materials to withstand temperatures of up to 2,000C (3,632F) resulting from a flight through the atmosphere at hypersonic speeds.
Earlier this week, Putin emphasized that Russia is the only country armed with hypersonic weapons.
He noted that for the first time in history Russia is now leading the world in developing an entire new class of weapons, unlike in the past when it was catching up with the United States.
The military said that the Avangard is capable of flying 27 times faster than the speed of sound.
Russian media reports indicated that the Avangard will first be mounted on Soviet-built RS-18B intercontinental ballistic missiles, code-named SS-19 by NATO.
It is expected to be fitted to the prospective Sarmat intercontinental ballistic missile after it becomes operational.
The Defence Ministry said last month that it demonstrated the Avangard to a team of US inspectors as part of transparency measures under the New Start nuclear arms treaty with the US.
The US has mulled new defence strategies to counter hypersonic weapons developed by Russia and China.
US officials have talked about putting a layer of sensors in space to more quickly detect enemy missiles, particularly the hypersonic weapons.
The administration also plans to study the idea of basing interceptors in space, so the US can strike incoming enemy missiles during the first minutes of flight when the booster engines are still burning.
The Pentagon also has been working on the development of hypersonic weapons in recent years, and US Defence Secretary Mark Esper said in August that he believes "it's probably a matter of a couple of years" before the US has one.
He has called it a priority as the military works to develop new long-range fire capabilities.