The assault marked Washington's first major military action in Yemen under President Donald Trump, who has vowed to step up the US fight against Islamic extremism.
The US military said the raid in the Yakla region of Baida province killed 14 members of Al-Qaeda in the Arabian Peninsula (AQAP), which Washington views as the global network's most dangerous branch.
A Yemeni provincial official gave a higher toll of 41 presumed militants and 16 civilians killed in the raid, including eight women and eight children.
"We are deeply saddened by the loss of one of our elite service members," said General Joseph Votel, commander of US Central Command in Tampa, Florida.
"The sacrifices are very profound in our fight against terrorists who threaten innocent peoples across the globe," Votel said.
A civil war in Yemen between Iran-backed rebels and pro-government forces has killed more than 7,000 people since March 2015 and allowed extremists including AQAP and the Islamic State group to gain ground in the impoverished nation.
Today's US raid was said to have targeted the houses of three tribal chiefs linked to Al-Qaeda.
The provincial official said Apache helicopters also struck a school, a mosque and a medical facility which were all used by Al-Qaeda militants.
The three prominent tribal figures killed in the attack were identified as brothers Abdulraouf and Sultan al-Zahab and Saif Alawai al-Jawfi, the official and other sources said.
They were known to be linked to Al-Qaeda, the sources said.
Awlaqi himself was killed in September 2011 in a drone strike and his son Abulrahman was killed two weeks later in a similar attack.
Local officials said an Al-Qaeda chief in the region was also killed in the raid.
The operation, which military authorities said resulted in the capture of information that would "provide insight into the planning of future terrorist plots", was the first major US military action in Yemen since Trump took office on January 20.
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