Ambiguity has a clear role in facilitating closure in negotiations to regulate natural resources. However, there are no empirical studies that examine whether such “constructive ambiguity” can in fact become destructive. The aim of the present study is thus to determine when ambiguity becomes destructive during the management phase of environmental regimes. The implementation of the Israeli-Jordanian water agreement is used as a case study. It was found that when political and hydrological conditions are unstable, the parties see the process of clarifying the ambiguities in a water agreement as broader than simply a question of bilateral relations over resource allocation. As a result, the cost of clarifying ambiguity at the implementation phase dramatically increases. The anatomy of resolving ambiguous agreements teaches us that there are early signs that indicate when ambiguity becomes destructive. Tracing these signals is crucial, since the cost of ambiguity is not linear. Rather, when a disagreement around ambiguity passes a threshold, it can escalate into a conflict in a very short time.