Dijkstal worked as a financial adviser, management consultant and civics teacher in Wassenaar from August 1967 until November 1982.

Dijkstal became a member of the House of Representatives after Wim van Eekelen was appointed as State Secretary for Foreign Affairs in the Lubbers I cabinet after the election of 1982, serving from 11 November 1982 until 3 June 1986.

Dijkstal returned to the House of Representatives after Ed Nijpels was appointed as Minister of Housing, Spatial Planning and the Environment in the Lubbers II cabinet after the election of 1986, taking office on 30 July 1986 serving as a frontbencher chairing the parliamentary committee for Petitions and the Citizen Initiatives and spokesperson for minorities and welfare.

Fortuyn blamed the problems in the country on the Purple cabinets (in which both Dijkstal and Melkert served as ministers).

[2][3] Dijkstal retired from national politics and became active in the private and public sectors and occupied numerous seats as a corporate director and nonprofit director on several boards of directors and supervisory boards (Institute for Multiparty Democracy, International Institute of Social History, Naturalis Biodiversity Center, Public Pension Funds APB and the Anne Frank Foundation) and served on several state commissions and councils on behalf of the government (Council for Public Administration, Kadaster and the Netherlands Film Fund) and as an advocate, lobbyist and activist for social justice and democracy.