The Israeli military first said it had killed Major General Mohammed al-Ghamari in an attack in August which killed the Prime Minister appointed by the Shi'ite group.
The Houthis did confirm his death until Thursday, and the date or details of his assassination were not immediately released.
"Appointed in 2016, al-Ghamari played a central role in building Houthi missile systems and weapons-production infrastructure, trained by Hezbollah and IRGC," the Israeli military said in a statement, referring to Iran's Revolutionary Guards.
"His elimination delivers a severe blow to the Houthi command structure, responsible for hundreds of attacks against Israel during the war."
At the mass funeral, Houthi politburo member Daifallah al-Shami praised the slain leader's role in confronting its enemies.
"Al-Ghamari and his comrades in the various formations of our armed forces played a great role in inflicting a humiliating defeat on America at sea, along with Britain, as well as on the criminal Zionist entity enemy over the course of two years," he said.