The Senate approved the measure as part of a massive defence spending bill that passed 86 to eight and already went through the House of Representatives, with President Donald Trump likely to sign it.
The United States imposed an embargo on the full island in 1987 with an aim to prevent an arms race and encourage a peaceful settlement between the Greek majority and Turkish minority.
Critics say the step has been counterproductive by forcing Cyprus to seek other partners while Turkey, a NATO member, has stationed forces in northern Cyprus since its invasion in 1974.
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Democratic Senator Robert Menendez and Republican Senator Marco Rubio spearheaded the effort, saying they also wanted to encourage growing cooperation between Cyprus, Greece and Israel.
"With Cyprus seeking to deepen its strategic partnership with the United States, it is in our national security and economic interest to lift this outdated decades-long arms restrictions that are no longer helping US security objectives," Menendez said after initial approval of the lifting of the embargo.
While the two Cypriot communities have made progress in improving relations, tensions have spiked over an accord between Turkey and Libya for newly discovered gas reserves in the eastern Mediterranean, undercutting claims by Greece and the internationally recognized Republic of Cyprus.
US officials have been concerned that the ban has brought EU member Cyprus closer to Russia, with the island in 2015 signing off on an access deal to its ports.
Under the new act, the United States will still restrict certain sensitive technologies to Cyprus unless the US certifies that the island is denying Russia military vessels port access for refuelling and servicing.
In a standoff in 1997, Turkey threatened an attack on Cyprus if it went ahead with installing the advanced S-300 missile defence system from Russia.
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The controversy is now a relic of another time, with Turkey facing the threat of sanctions for buying the S-400 system from Russia despite its NATO membership.
Representatives of Turkey and the self-styled Turkish Republic of Northern Cyprus had lobbied against the lifting of the embargo, arguing that Congress was giving the green light to an arms race.
Turkey invaded in 1974 in response to a coup engineered by the then military regime in Athens that aimed to unite Cyprus with Greece.
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