Iran-backed Houthi rebels have previously attacked shipping in the vital sea trade corridor to disrupt Israel's retaliatory strikes on Gaza following the October 7 Hamas attack.
The Defence department on Friday announced Australia will assume command of Combined Task Force 153 (CTF 153) from October for six months.
Established in April 2022, CTF 153 focuses on maritime security in the Red Sea, Bab al-Mandeb and Gulf of Aden.
The Albanese government last year was criticised by security experts for declining a US request to deploy a warship to protect maritime security in the Middle East.
Australia will maintain its contribution to the Combined Maritime Force, which was strengthened last December in response to Houthi attacks, the ADF said on Friday.
Chief of Joint Operations Vice Admiral Justin Jones said the role demonstrated the nation's commitment to international rules.
"Australian Defence Force command of CTF 153 is a significant milestone in our commitment to maritime safety and security," he said.
"We proudly work alongside 44 other member nations in the Combined Maritime Force to support freedom of navigation and free, fair and open trade, and the international rules‑based order."
Australian National University expert associate Jennifer Parker said the command would provide Australian forces with experience that might be relevant for other areas of operation.
"Taking command will provide Australian Navy personnel good experience in operations to protect maritime shipping through key maritime choke points - a task that will be highly relevant to Australia's national security in the event of a crisis or conflict in the Indo-Pacific," she told AAP.
"As the maritime domain becomes more contested, it is important as a maritime nation that Australia develops and maintains the ability to respond to crisis' that impact maritime trade."
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