Cahill made his breakthrough in the professional game with the London club before securing a move to Everton in 2004, where he enjoyed eight seasons as a key player for the Toffees.
The 38-year-old has since played in Major League Soccer and the Chinese Super League while remaining an integral part of the Socceroos setup.
Cahill's decisive brace secured a place at Russia 2018 as Australia overcame Syria 3-2 on aggregate in November, but he left Melbourne City last month citing a lack of game time, which he feared might place his World Cup spot in jeopardy.
He has agreed a deal running until the end of the Championship season at Millwall under his old team-mate Neil Harris, although he will not be eligible for Wednesday's (AEDT) game against promotion-chasing Derby County.
"It's hard to put into words," said Cahill in an interview with Millwall's official website. "I'm still taking it in now.
"The first thing I wanted to do was to walk on the pitch and in the tunnel and have that feeling again. That brings back so many memories.
"Once you go over that white line, you get a nervous sensation back that I had when I was a 16-year-old when I first signed here.
"I'm really happy. I've had a great career as a footballer, but to come here now at this stage of my career, with eyes on a World Cup place, it's such a professional environment. It's familiar. Not much has really changed, which is surprising, but it's nice to come back to where I was as a kid."
Cahill said: "The romance of the story is definitely not lost on me. I've always said that if I came back to England, I'd come home. Millwall is where I learnt my trade and it was the most important learning period of my life – my apprenticeship in understanding football.
"To come home to where it all started, it's emotional, but it's happy emotions because you wish for it to happen, you want it to happen. When it finally comes to fruition, it's the perfect move."
Cahill has represented his country at the last three World Cups, becoming the first Australian to score a goal in the competition at the 2006 tournament in Germany.
His tally of 50 international goals is a record for Australia.