James Murdoch has been succeeded by Nicholas Ferguson, who previously served as Deputy Chairman of BSkyB and was appointed a director in 2004.
He thanked Mr Murdoch for his "vision, drive and strategic insight" and said he had made an "outstanding contribution" to the company.
He has been chairman of private equity firm SVG Capital Plc since 2005 and is also Chairman of the Courtauld Institute of Art.
In a joint statement, Rupert Murdoch and News Corp president Chase Carey said: "We look forward to BSkyB's continued growth under the leadership of Nicholas Ferguson".
James Murdoch says he resigned to stop BSkyB from being tainted by the phone hacking allegations levelled at News International.
The MPs' report into phone hacking is likely to accuse some witnesses of misleading Parliament. Will James Murdoch be among them?