The Potters sacked Steven Schumacher in the aftermath of their 1-0 defeat at United on Saturday, and have appointed former Norwich City first team coach Narcis Pelach as their new boss.
Abingdon-born Whitehead joins the Potters having only joined the backroom staff at Barnsley in July.
Since hanging up his boots, Whitehead has held coaching roles at Huddersfield Town, Shrewsbury Town, Port Vale, Besiktas, Cardiff City and Watford.
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The U’s youth product made 136 appearances for the club, scoring nine goals, before joining Sunderland in June 2004.
Whitehead spent five years at the Stadium of Light, and was twice a Championship winner with the Black Cats.
He joined the Potters for £3 million in July 2009, and made 158 appearances, including as a substitute in the 1-0 FA Cup final defeat to Manchester City in 2011.
Whitehead spent the final five years of his career with Middlesbrough and Huddersfield, and when he retired, he boasted 620 appearances on his CV, including 234 in the Premier League.