Flanker Hooper has captained Australia on 68 occasions and returns to the role less than 12 months after walking out on the Wallabies ahead of their Rugby Championship opener saying he was not in the right frame of mind to play.
Experienced prop Slipper, who has won 127 caps for his country, stepped up to replace Hooper after his abrupt departure and has captained Australia 12 times.
Jones, who replaced Dave Rennie as coach in January, said his decision to go for co-captains was inspired by a visit to the Sydney Swans Australian Rules team.
"They've got a tradition of co-captaincy and I just wanted to delve down into the area of the advantages and disadvantages," Jones said after announcing his squad on Channel Nine.
"I think with Slips and Hoops, we cover the range of the squad. Both have a slightly different approach to leadership, both have got a slightly different approach to the way they play the game, and I think together, they can be a really strong captaincy group."
Jones also named a 34-man squad for the Rugby Championship, with hooker Matt Faessler, prop Zane Nonggorr and flanker Josh Kemeny the most surprising selections among the eight uncapped players.
Less surprising were the inclusions of flyhalf Carter Gordon, locks Tom Hooper and Richie Arnold, winger Dylan Pietsch and scrumhalf Ryan Lonergan, who have all had strong campaigns at club and provincial levels.
The most notable absentee was flyhalf Bernard Foley, who returned from international exile to start Australia's final six tests of last season.
"It's probably one of the hardest squads I've had to select," said Jones, who previously coached Australia from 2001 to 2005.
"The back row was tight, standoff was tight, halfback was tight. So there were a few sleepless nights.
"We know that in the Rugby Championship and in the World Cup, we'll have at least a 20% injury rate so there'll be opportunities for players who missed out."
The former England coach has also been given approval by Rugby Australia to utilise five overseas-based players for the Rugby Championship, instead of the usual three.
Centre Samu Kerevi, who is not yet available for selection because of injury, winger Marika Koroibete, locks Will Skelton and Richie Arnold as well as flyhalf Quade Cooper were the players selected.
Australia's Rugby Championship campaign gets underway against South Africa in Pretoria on July 8.
