Faulkner, who has been a part of IPL in 2011 (Pune Warriors), 2012 (Kings XI Punjab) and 2013 (Rajasthan Royals), has stood in 19 ODIs for the Aussies and played a single Test.
CA 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."
"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.