The Department for Culture, Media and Sport announced today that Serota had been appointed to the role for a term of four years, replacing Sir Peter Bazalgette at the end of his four years.
A Tate spokeswoman said Serota, who will take up his new role on 1 February, was initially expected to carry out both roles concurrently until his successor at the Tate was appointed.
Serota will be paid £40,000 a year for approximately two days a week.
He said: "This is an enormous honour, given the 70-year history of the council, its success in recent years and the crucial role that it plays in promoting art and culture in this country."
Karen Bradley, the culture secretary, said Serota had transformed the Tate during his time there.
"He brings unparallelled experience, creativity and wisdom and will continue to be an enthusiastic champion of the arts in his new role," she said.
Arts Council England will invest £1.1bn from government and an estimated £700m from the National Lottery in art and culture between 2015 and 2018.