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 across the bridge, which links the Taman peninsula in southern Russia 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, historic 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.
The Russian leader, who was re-elected for a fourth Kremlin term in March extending his long rule, 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 (USD 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.
Ukraine, which along with most of the international community has not recognised Russia's annexation of Crimea, condemned the project which was personally championed by Putin.
The European Union also criticised what it called a fresh assault on Ukraine's territorial integrity.
"This constitutes another violation of Ukraine's sovereignty and territorial integrity by Russia," said a statement by a spokesperson for the office of the European Union's foreign policy service, which said the bloc continues to refuse to recognise Russia's annexation of Crimea.
Meanwhile, Ukraine's security service raided the offices of Russian state media in Kiev and detained one local journalist on suspicions of treason, moves the chief editor of Russia's RT television suggested were linked to the bridge opening.
The chief editor of the Kremlin-funded channel, Margarita Simonyan, wrote on Twitter that "Kiev decided to take revenge on us for the Crimean Bridge," after the raids on the offices of RIA Novosti state news agency, which is part of the same media group as RT.
European Union and US sanctions have targeted those involved in building the bridge, principally Putin's close ally, businessman Arkady Rotenberg, whose company Stroygazmontazh won the construction contract.
The annexation of the peninsula in 2014 was condemned by Kiev and the West as an illegal land grab but applauded in Russia.
(This story has not been edited by Business Standard staff and is auto-generated from a syndicated feed.)