Sir Nicholas Serota is stepping down as director of the Tate.
Sir Nicholas, who has transformed the success of the Tate, has been announced as the new chairman of Arts Council England.
The announcement follows a wave of resignations in the art world.
Sir Nicholas has been at the Tate for 28 years and was the force behind the creation of Tate Modern, which became the most popular modern art museum in the world, while rebranding the original gallery at Millbank as Tate Britain.
Contemporary art gallery Tate Modern recently opened a new wing following a £260 million redesign.
Sir Nicholas said that his period at Tate had been "an exciting challenge" and that there had been a "sea-change in public appreciation of the visual arts in this country" during the last 30 years.
He will take up the part-time, £40,000 role at the Arts Council in February for a term of four years, replacing Sir Peter Bazalgette in the role.
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."
His announcement comes after the director of the Victoria and Albert (V&A) Museum, Martin Roth, announced he was stepping down after five years in the role.
The German-born 61-year-old said that it had been a "privilege and tremendously exciting" to be at the helm of the museum, which featured shows such as David Bowie is and Alexander McQueen: Savage Beauty, during his period in charge.
He had expressed his concern at the Brexit vote in July, telling the BBC it was "unknown" and felt like "skiing in very thick fog".
Neil MacGregor stepped down as director of the British Museum at the end of December 2015, and was replaced by Dr Hartwig Fischer.
Sir Nicholas recently spoke about how he felt that leaving the European Union would diminish the work of Tate Modern.
He told the Press Association before the June 23 poll: "This is a museum that presents its face to the world, and it has enjoyed particular collaborations with European colleagues... Anything that makes that more difficult would, I think, diminish the quality of what we are able to show and do here."
Asked what he would do if Britain voted to leave, he said: "There's not really a contingency plan, we'll have to see what happens."
Sir Nicholas, now 70, made his name at the Whitechapel Gallery, when he landed a role as its director in 1976 and presented early exhibitions by the likes of Antony Gormley and Tony Cragg during his 12 years there.
He went on to co-curate a major Royal Academy show in 1981, A New Spirit In Painting, and was appointed director of Tate in 1988, becoming its longest serving director.
Under his leadership, the Turner Prize became famous and hit the headlines for its controversial winners, including Damien Hirst's bisected cow and calf preserved in formaldehyde and Martin Creed's light going on and off.
Tate Modern drew crowds to its Turbine Hall installations, including Olafur Eliasson's dazzling sun and Carsten Holler's slide installation, while Tate Britain and Tate Modern were linked by a Tate boat service.
The process of finding a new director will begin immediately.
Arts Council England provides funding for a range of arts activities.
One of Sir Nicholas's first jobs was at the Arts Council of Great Britain, as a regional art officer in 1970.