Russian state television showed Putin dressed in jeans and a casual jacket sit behind the wheel of a construction truck with workers to drive 19 kilometres (12 miles) across the bridge, which links the Taman peninsula in southern Russian to Ukraine's Crimea peninsula annexed by Moscow in 2014.
"I want to sincerely congratulate you with this remarkable, festive and, in the full sense of the word, historical day," Putin told workers upon arrival on the Crimean side of the bridge.
"In different historical eras, even under the tsar, people were dreaming of building this bridge," Putin told cheering workers.
He was referring to Russia's last tsar, Nicholas II, who first proposed such a bridge, but the outbreak of World War I prevented it going ahead.
Another unsuccessful attempt was made in the 1930s under Joseph Stalin. During World War II the occupying Nazis also began building a bridge but abandoned the project.
"And finally, thanks to your work, your talent, this project, this miracle happened!" Putin said.
The Russian leader, who was re-elected for a fourth Kremlin term in March extending his long rule, then pledged to build more of "such projects" across Russia.
The Crimean Bridge overtakes Lisbon's Vasco da Gama Bridge as the longest in Europe.
Built at a cost of 228 billion rubles ($3.7 billion), the new structure connects the southern Krasnodar region with the Crimean city of Kerch, spanning a strait between the Black and Azov seas.