The posts include the new First Civil Service Commissioner, who will be outside the service and charged with maintaining "the ethics and standards of a politically impartial permanent civil service".
The other is for a permanent secretary at the Department of Employment, running a £4.6bn budget and 58,000 staff.
The salaries are £95,000, pro rata for the part-time commissioner, but set to rise and are subject to negotiation for "an outstanding candidate".While some posts at permanent-secretary level have been advertised before, previous examples have been for specialists such as the Chief Medical Officer and Chief Economic Adviser to the Treasury. The employment post is the first at the policy core of the service to be advertised.
The move follows criticism from the cross-party Treasury and Civil Service Select Committee that the senior civil service remains too insular and Oxbridge-dominated.
The advertisements may herald a pay explosion. Some heads of civil service agencies are already paid far more than the permanent secretaries to whom they report. Derek Lewis, head of the Prison Service, received £125,000 and a £35,000 bonus last year, while John Chisholm, earns £147,000 as head of the Defence Research Agency, £88,000 more than his Civil Service predecessor.
Successful outsiders have tended to command higher salaries.
Giles Radice, chairman of the civil service Select Committee, backed the move, while saying that most appointments should remain internal. "The top civil service should be opened up to competition, but we need a code and an appeal system to ensure politicisation of the civil service does not follow."
The First Division Association, the top civil servants' union, said it was baffled by the criteria used to decide which posts were advertised.