Putin annexed Crimea, a Ukrainian peninsula in the Black Sea, in 2014, after claiming that ethnic Russians in the region were threatened by Ukraine's pro-Western revolution.
When they were still friends, back in 1994, Russian Federation and Ukraine tried to work together on a bridge project, but this idea failed too.
The peninsula has until now been hard to access from southern Russian Federation with long queues of vehicles often trying to board ferries, which are not always able to run during winter storms.
"In different historical eras, even under the tsar, people were dreaming of building this bridge", Putin told cheering workers.
"Russia's construction of the bridge serves as a reminder of Russia's ongoing willingness to flout worldwide law", State Department spokeswoman Heather Nauert said.
US Department of State Spokesperson Heather Nauert told reporters on Tuesday that the construction allegedly impedes navigation and "limits the ability to bring in goods via ship".
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The controversial bridge became Europe's longest bridge and provides direct access to Russia's mainland. "We call on Russian Federation not to impede this shipping", she said.
About 10,000 workers participated in the work, a figure that at peak moments of the construction works reached the 15,000, while some 220 national companies contributed to the so-called work of the century, said the president visibly moved.
Putin thanked the organizers of the project, who put the interests of the state over those of particular groups, the sappers, ecologists, scientists and other sectors involved.
On May 15, Russian Federation officially opened the bridge across the Kerch Strait to the occupied Crimea.
"Today, both in a practical sense and from a symbolic point of view, is an extremely important day", he added.
On March 18, President Vladimir Putin signed the treaty on Crimea's reunification with Russian Federation and the Federal Assembly (parliament) approved the document on March 21.
The bridge has two layers carrying cars on top and a railway underneath.