The USS Lassen's patrol was the most significant US challenge yet to the 12-nautical-mile territorial limits China claims around artificial islands it has built up in the Spratly archipelago as Beijing exercises its growing maritime power.
Washington's move followed months of deliberation by the administration of President Barack Obama and could ratchet up tension in one of the world's busiest shipping lanes and increase strains in US-China relations.
A US defense official said the Lassen also went within 12-mile limits of features in the disputed sea claimed by Vietnam and US treaty ally, the Philippines. They said such "freedom-of-navigation" patrols were expected to become more frequent.
The US destroyer sailed within 12 nautical miles of Subi Reef, an artificial island built up by China in the past year.
A Chinese guided-missile destroyer and a naval patrol ship shadowed and gave warnings to the US warship "according to law", China's Defense Ministry said.
The US patrol was a "coercive action that seeks to militarize the East Sea region" and an "abuse" of freedom of navigation under international law, it added.
US Defense Secretary Ash Carter, testifying on October 27 to the Senate Armed Services Committee, initially would only say the US Navy had conducted operations in the East Sea. But under questioning from lawmakers, he said the USS Lassen had passed within 12 miles of a Chinese artificial island.
China's Vice Foreign Minister Zhang Yesui summoned US Ambassador Max Baucus, telling him that the patrol was "extremely irresponsible," the Foreign Ministry said. It earlier said the USS Lassen "illegally" entered waters near islands and reefs in the Spratlys without the Chinese government's permission.
"China will resolutely respond to any country's deliberate provocations," the ministry said in a statement that gave no details on precisely where the US ship sailed.
Foreign Ministry spokesman Lu Kang told a daily briefing that if the United States continued to "create tensions in the region," China might conclude it had to "increase and strengthen the building up of our relevant abilities".
Lu did not elaborate, except to say he hoped it did not come to that, but his comments suggested China could further boost its military presence in the East Sea.
In Washington, US State Department spokesman John Kirby told a regular briefing that "Setting this aside, the US-China relationship is vitally important and one we want to see continue to improve and to grow for the benefit of both our countries, not to mention the region."