International organizations (IOs) are challenged by their most powerful member states which increasingly attack their fundamental purposes. Yet, we know little about how and under which conditions IO bureaucracies respond to their contestation. Some choose to avoid public conflict by ignoring the contestant, whereas others try appeasing them; yet others react by blurring their position, whilst some even respond by attacking the contestant. We argue that, when responding to contestation, IO administrations are confronted with the Agent’s Dilemma: they must sustain crucial support from the dissatisfied power; while at the same time maintaining their reputation for advocating their IO’s purpose in the eyes of other members and stakeholders. Which response IO administrations chose to navigate the Agent’s Dilemma is shaped by (1) their involvement in IO policymaking; and (2) their IOs’ dependency on the contesting state. We assess these expectations by, first, assessing the two conditions across 42 instances of IO administrations’ responses to contestation by the Trump Administration, and, second, employing interview data to study the responses of NATO, WTO, UNHCR, and UNEP in more depth. Our results point to the potential of strong bureaucracies in defending their IOs’ purposes even against their most powerful member states.