Cortnee Vine and Katrina Gorry also feature in a 24-player squad announced on Friday.
Kerr last played for Australia in November, 2023, having endured a horror 20-month rehabilitation from an ACL tear suffered at a Chelsea training camp in January 2024.
The superstar striker returned for the Blues last month, scoring her 100th goal for the club in her first game back.
"Having Sam back in the squad is a special moment - not just for the team, but for Australian football," Matildas coach Joe Montemurro said in a statement.
"Her leadership and presence are invaluable as we continue building toward the AFC Women's Asian Cup 2026 and beyond."
Vine, the penalty shootout hero for Australia at the World Cup, is in the national squad for the first time since the Paris Olympics.
A mental-health break, injuries and a difficult start to life in the NWSL with North Carolina Courage had kept her out of the Matildas.
Gorry is due to play for the first time under Montemurro, after missing his first window through personal leave.
"The squad showcases the depth we are looking to build, by utilising experienced players who continue to set high standards alongside the next generation of Matildas players," Montemurro said.
"It will be Australia's first time competing against Wales and there is a competitive history with England, so both games will provide different challenges to test the team, our playing style and the way we play together."
Australia will play Wales at Cardiff City Stadium on October 25 (local time) and England at Derby's Pride Park three days later.
Kerr has been on limited minutes at Chelsea and is likely to be gradually introduced in those games.
The 32-year-old previously joined Matildas camps in a non-playing capacity as part of her rehabilitation.
It is unclear whether Kerr will retain the captaincy, with Steph Catley donning the armband during her absence with aplomb.
Forward Mary Fowler (ACL) and midfielder Tameka Yallop (hamstring) remain unavailable.
The most recent meeting between Australia and England came in the semi-final of the 2023 Women's World Cup in Sydney.
Although England prevailed 3-1, Kerr produced one of the highlights of the tournament with a brilliant solo goal in the 63rd minute which levelled scores at 1-1.
Kerr missed the entire group stage after tearing her left calf on the eve of the tournament.
She later revealed she tore her right calf during the 2-0 loss to Sweden in the third-placed play-off.
Australia are hosting the 2026 Women's Asian Cup, starting on March 1, and a fully fit Kerr looms as vital to the Matildas' silverware hopes.
The Matildas bombed out in the group stage of the Paris Olympics without Kerr, but hopes are high Australia can win the Asian Cup on home soil.
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