The "Neva" toll road, running 669 kilometres (416 miles) and named after Saint Petersburg's main river, is Russia's first long-distance toll road.
It boasts no traffic lights and a higher maximum speed limit of 130 kilometres per hour (81 miles per hour) versus 110 kph on other roads.
"We've never had anything like this in our country's history, in the history of road construction," said Putin, who grew up in Saint Petersburg. "Now we do."
National media reported that the five-and-a-half to six-hour drive will beat most commuter trains for the first time.
"I used to take the old road, the M10, it took 10 hours," Putin said. Transport Minister Yevgeny Ditrikh added: "And that was the best case scenario."
"You can really drive it in six hours," said state-owned daily Rossiiskaya Gazeta after a test drive.
Putin nevertheless flew to the city, local media noted.
The project suffered years of controversy as environmentalists protested against the route through the Khimki forest near Moscow.
Mikhail Beketov, editor of the Khimki newspaper, who campaigned against the construction, was brutally beaten and died in 2013.
One of the most prominent activists opposing the motorway, Yevgeniya Chirikova, had to flee the country.
High-speed trains between the cities are still quicker, at around four hours but are relatively expensive.
The new motorway toll costs up to 2,020 rubles ($32) per car.
First mooted in 2006, construction reportedly cost 495 billion rubles ($7.7 billion), including private investment.
French group Vinci took part in the project in a consortium with Russia's VTB Bank.
AFP
More about: Russia
