Former AOL chief executive Miller joined News Corporation in 2009 and oversaw the ill-fated relaunch of MySpace.
News Corp gave up on the MySpace turnaround bid and sold the company last June to Specific Media, with News Corp chairman and chief executive Rupert Murdoch saying, "we screwed up in every way possible, learned lots of valuable, expensive lessons".
Miller has also overseen projects including the launch of digital magazine The Daily and the partnership with video service Hulu, where he was also on the board of directors.
News Corp stated that Miller was "instrumental" in strengthening relationships with the technology industry and has credited him for overseeing key investments, including the recent stakes taken in streaming site Roku and Bona Film Group.
Miller was brought in to steer News Corp’s digital strategy, which has seen it move away from standalone web properties, to refocus on digital content distribution and the monetization of existing brands on emerging platforms.
The departing executive said it felt "like the right time to exit" and added he was looking forward to new ventures that "will lead me back into an operational role".
News Corp will keep Miller on as an "outside adviser" on digital issues through to autumn 2013.
Murdoch said: "Jon Miller is a visionary in the digital media industry, and his commitment to News Corporation over the last three years has driven us to truly evolve the way millions of people use new platforms to consume news and entertainment.
"As we prepare for our proposed company separation, I respect Jon's desire to return to an operational, entrepreneurial role with a standalone company. He will be missed and I can'' thank him enough for his efforts and many valued contributions."