The change comes as Sir Bob Kerslake announced his plan to step down as head of the home civil service in the autumn and to retire as permanent secretary of the Department for Communities and Local Government in February 2015.
The role of head of the home civil service will be handed to Downing Street's top official, Cabinet Secretary Sir Jeremy Heywood, and the new chief executive will report to him once appointed.
The move tears up reforms introduced by Mr Cameron in 2011, when he split the roles of Cabinet Secretary, head of the Home Civil Service and permanent secretary at the Cabinet Office. But Downing Street rejected suggestions that it was a mark that the previous changes had failed.
The new chief executive will also run the Cabinet Office, though it unclear if he or she will also have the title of permanent secretary of the department. Current permanent secretary Richard Heaton will remain first parliamentary counsel.