Koenders was adjunct professor at Webster University in Leiden from 1987 to 1993. In 2002 he was visiting professor at Johns Hopkins University in Bologna teaching about conflict prevention and management, and post-conflict reconstruction. Due to his past experience of being a professor, he occasionally participates in lectures about specific aspects of political science at various universities around the Netherlands. From 1983 to 1993, Koenders worked as an aide for the Labour Party in the House of Representatives. He served as an adviser to the United Nations Operation in Mozambique in the early 1990s, his first job outside the Netherlands. Between 1995 and 1997, he worked in the private office of Hans van den Broek, who was then the Dutch European commissioner and had shared responsibility for foreign policy. During that time, one of his tasks was defining the EU’s competences on foreign policy. , Rwandan general Jean Bosco Kazura, Special Representative Bert Koenders and Minister of DefenceJeanine Hennis-Plasschaert in Bamako on 28 November 2013. John Kerry at a NATO summit in Brussels on 2 December 2014.
Koenders was a member of the House of Representatives from 1997 until 2007. In 1997, he filled the vacant seat after member of parliament Maarten van Traa died in a car accident. He was member of the permanent parliamentary committees on foreign affairs and on defense. From 2002 until 2003 he was a member of the parliamentary hearing committee on the Srebrenica massacre. From 17 November 2006 to 19 February 2007 he was president of the NATO Parliamentary Assembly.
Koenders was minister without portfolio for Development Cooperation in the Fourth Balkenende cabinet sworn in on 22 February 2007. He came under political fire as minister in July 2007, after it became known that an event sponsored by the Ministry, Het akkoord van Schokland, was organized without a public procurement process stipulated under European Union law. Instead, the event was organized by an event bureau closely tied to the Labour Party itself. Koenders cited time shortage. Between 2008 and 2009, Koenders was part of a High-Level Taskforce on Innovative International Financing for Health Systems, which had been launched to help strengthen health systems in the 49 poorest countries in the world and was chaired by UK Prime Minister Gordon Brown and World Bank presidentRobert Zoellick. In 2009, he criticized Pope Benedict XVI for his assertion that distributing condoms is not the solution to AIDS and actually makes the problem worse.
On 17 October 2014, Koenders succeeded Frans Timmermans as Minister of Foreign Affairs. At the 2016 United Nations Security Council election, Koenders and his Italian counterpart Paolo Gentiloni agreed on splitting a two-year term on the United Nations Security Council after the United Nations General Assembly was deadlocked on whether to choose Italy or the Netherlands following five rounds of voting for the last remaining 2017/18 seat. In December 2016, Koenders summoned Sadık Arslan, Turkey's ambassador in the Netherlands, after the De Telegraaf newspaper reported that the Turkish embassy had sent home a list of Dutch Turks who might have sympathized with the failed coup.