The much-anticipated concerts in late 2027 will mark the group's first tour in 17 years, with each performance held in a stadium-sized big top.
The concerts will be all ages, with both seated and standing tickets available, and fan pre-sales are set to start Wednesday morning.
Making the announcement on Monday, the band members revealed that many of their long term fans had never seen them play a live show - including their own kids, who were too young to experience Powderfinger's heyday in the 2000s.
"People often tell us that our music is connected to their most treasured and joyous memories," Powderfinger said in a message emailed to fans.
"We hope to spread a little more of that joy when we make our way around the country with some of Australia's best established and upcoming talent, and to make some new memories for us all."
They will kick off in their hometown of Brisbane for four shows over two weeks at the Brisbane Showgrounds from September 3.
From there, they will head north for two shows at Cairns' Cazaly's Stadium, before heading west for another two gigs at Perth's Wellington Square.
The big top will then touch down at the Domain in the heart of Sydney for four shows from October 1 to 9.
Adelaide's Ellis Park will host another two shows in mid-October, before Melbourne's Park Oval rounds out the tour with four dates from October 22 to 30.
With more than two million album sales and 18 ARIA awards to its name, Powderfinger is among Australia's best-loved acts.
Formed in the Queensland capital in 1989, Powderfinger developed its sound amid the grunge era of the early 1990s.
National acclaim first came with their second album, Double Allergic, which peaked at number four on the ARIA charts.
Their next five studio albums, from Odyssey Number Five in 2000 to Golden Rule in 2009, all soared to the top spot.
But some 17 years will have passed since the group closed the aptly-named Sunsets Farewell tour in their hometown of Brisbane in 2010.
The band confirmed the tour on Friday with a video statement shared to social media, which dominated headlines and ended days of speculation.
"We always said that if we were going to get back together to do some shows that you guys would be the first to know," said frontman Bernard Fanning.
"Now, you're the first to know."
The teaser campaign started days before, with billboards in capital cities featuring grids of numbers and letters referencing their discography and the date of their final live show in Brisbane in 2010.
General ticket sales start from Monday, October 19.