It is the first time the Wallabies have installed two captains, with the inspirational Hooper now appointed leader of the national side under four separate coaches.
"Michael and James are both world-class players, strong leaders and embody what it means to be a Wallaby," said Jones in announcing their appointment through 2023 among a 34-man squad for the Rugby Championship.
"They have worked hard with the leadership group since January, and it will be important they continue to have strong support from the players around them."
Flanker Hooper, who spent two months out of the game on a mental health break last year, relinquishing the captaincy to prop Slipper, is Australia's most-capped skipper, having led the side in 68 of his 124 Tests.
Slipper also brings vast experience, with his 127 Test appearances third on the all-time Wallabies list behind George Gregan (139) and Stephen Moore (129).
"It's an absolute honour to lead the squad alongside Slips," said Hooper.
"We've been having great discussions as a leadership group and wider squad throughout the year and there's a really optimistic mindset as a collective heading into what's a massive four months."
Australia face South Africa in Pretoria on July 8, and Argentina a week later in Sydney, before two Bledisloe Cup fixtures with the All Blacks ahead of their departure for the September-October World Cup in France.
Jones, who took the reins from Dave Rennie in January, named eight uncapped players in the squad, with Melbourne Rebels duo Carter Gordon and Josh Kemeny rewarded, along with Queensland Reds front-rowers Matt Faessler and Zane Nonggorr.
ACT Brumbies teammates Tom Hooper and Ryan Lonergan also earned call-ups, as did NSW Waratahs flyer and former Australia Sevens representative Dylan Pietsch.
Towering lock Richie Arnold was the final uncapped player, having helped Stade Toulouse win the Top 14 in France.
He was one of five overseas-based stars named, along with experienced winger Marika Koroibete, fly-half Quade Cooper and centre Samu Kerevi, all of whom play in Japan, as well as La Rochelle lock Will Skelton.
Under the so-called "Giteau's Law", Australia only permits three overseas-based players to be picked, but Jones sought approval for two more, which was granted by Rugby Australia.
One of the biggest omissions was Japan-based playmaker Bernard Foley, who started the last six Tests.
"Getting selected in the squad is just the start," said Jones. "We've got to build the team now and that will require hard work and getting a little bit more out of everyone involved."
Wallabies squad:
Allan Alaalatoa (ACT Brumbies), Richie Arnold (Stade Toulouse, (Matt Faessler (Queensland Reds), Nick Frost (ACT Brumbies), Matt Gibbon (Melbourne Rebels, Jed Holloway (NSW Waratahs), Michael Hooper (co-captain, NSW Waratahs), Tom Hooper ( ACT Brumbies), Rob Leota (Melbourne Rebels), Fraser McReight (Queensland Reds), Zane Nonggorr (Queensland Reds), David Porecki (10 Tests), Pete Samu (ACT Brumbies), Will Skelton (La Rochelle), James Slipper (co-captain, ACT Brumbies), Taniela Tupou (Queensland Reds), Jordan Uelese (Melbourne Rebels), Rob Valetini (ACT Brumbies), Quade Cooper (Kintetsu Liners), Lalakai Foketi (NSW Waratahs), Carter Gordon (Melbourne Rebels), Reece Hodge (Melbourne Rebels), Len Ikitau (ACT Brumbies), Marika Koroibete ( Saitama Wild Knights), Ryan Lonergan (ACT Brumbies), Tate McDermott (Queensland Reds), Mark Nawaqanitawase (NSW Waratahs), Izaia Perese (NSW Waratahs), Suliasi Vunivalu (Queensland Reds), Nic White (ACT Brumbies), Tom Wright (ACT Brumbies), Ben Donaldson (NSW Waratahs), Josh Kemeny (Melbourne Rebels), Dylan Pietsch (NSW Waratahs), Angus Bell (NSW Waratahs), Langi Gleeson (NSW Waratahs), Andrew Kellaway (Melbourne Rebels), Samu Kerevi (Urayasu D-Rocks), Jordan Petaia (Queensland Reds), Matt Philip (Melbourne Rebels)
