The vessel passed close to Triton Island in the Paracel Islands, a statement said.
China, one of the countries claiming the islands, responded by accusing the US of violating its laws.
China and several other nations have rival claims in the South China Sea, which is rich in resources.
The US says it does not take sides on such territorial disputes but wants to safeguard access to the important shipping route.
'No prior permission'
The mission aimed at countering "excessive maritime claims of parties that claim the Paracel Islands", the Pentagon said.
"This operation challenged attempts by the three claimants - China, Taiwan and Vietnam - to restrict navigation rights and freedoms," around the islands, said spokesman Capt Jeff Davis.
According to the statement, the USS Curtis Wilbur destroyer sailed within 12 nautical miles of Triton Island. No Chinese vessels were in the area at the time, the Pentagon said.
But a Chinese foreign ministry accused the US of violating Chinese law "by entering Chinese territorial waters without prior permission".
The US admitted it had not notified any of the claimants prior to the mission but this was "consistent with our normal process and international law".
In a previous "freedom of navigation" operation, the US sailed a destroyer close to the disputed Spratly Islands last year, an incident that also sparked a protest from China.
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