Unlike other primitively eusocial wasps, Ropalidia marginata colonies are usually headed by remarkably docile and behaviourally non-dominant queens who are nevertheless completely successful in maintaining reproductive monopoly. As in other species, loss of the queen results in one of the workers taking over as the next queen. But unlike in other species, here, the queen's successor cannot be predicted on the basis of dominance rank, other behaviours, age, body size or even ovarian development, in the presence of the former queen. But the swiftness with which one and only one individual becomes evident as the potential queen led us to suspect that there might be a designated successor to the queen known to the wasps, even though we cannot identify her in the queen's presence. Here, we present the results of experiments that support such a 'cryptic successor' hypothesis, and thereby lend credence to the idea that queen (and potential queen) pheromones act as honest signals of their fertility, in R. marginata.