Faulkner, who played in the Indian Premier League in 2011 (Pune Warriors), 2012 (Kings XI Punjab) and 2013 (Rajasthan Royals), has stood in 24 ODIs for the Aussies and played a single Test.
Cricket Australia chairman of selectors Rodney Marsh expects Faulkner, 24, to perform well.
"James is a young man with plenty of character and possesses a great desire to win," Marsh said.
"He is still developing as an all-rounder but we believe this captaincy provides him an opportunity to do that as well as develop his leadership skills."
Meanwhile, middle-order batsman Cameron White will lead the one-day squad in a quadrangular series post the two unofficial Tests.
Marsh believes White's huge experience in limited-overs cricket will benefit the ODI team.
"Cameron White has been selected as captain of the one-day team for the quad series in Darwin. Cam White is a very good captain with loads of experience and will set a fine leadership example to the younger players," Marsh said.
Some known Australian players, including Josh Hazlewood, Moises Henriques, Phillip Hughes, Chris Lynn and Mitchell Marsh are part of both the sides.
Australia A take on India A in two four-day matches from July 6-17 in Brisbane, then move to Darwin for the one-day series from July 19 - August 2 before concluding with two four-day matches against South Africa A in Townsville from August 7-17.
Squads:
Four-day matches vs India A, Brisbane
Cameron Boyce, Ben Cutting, Alex Doolan, James Faulkner (captain), Peter Forrest, Josh Hazlewood, Moises Henriques, Phillip Hughes, Chris Lynn, Mitchell Marsh, Kane Richardson, Chadd Sayers, Sam Whiteman
One-day matches in Darwin and Palmerston.
Cameron Boyce, Pat Cummins, Ben Cutting, Alex Doolan, Callum Ferguson, Josh Hazlewood, Moises Henriques, Phillip Hughes, Chris Lynn, Mitchell Marsh, Clink McKay, Peter Nevill, Kane Richardson, Cameron White (captain).
Four-day matches vs South Africa A, Towsnville
Jason Behrendorff (subject to fitness), Tom Cooper, Ben Cutting, James Faulkner (captain), Callum Ferguson, Peter Forrest, Josh Hazlewood, Moises Henriques, Phillip Hughes, Chris Lynn, Peter Nevill, Steve O'Keefe (subject to fitness), Chadd Sayers.
Image: James Faulkner
Photograph: Scott Barbour/Getty Images
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