Significance Both the role of host sanctions (differential resource allocation to more beneficial symbionts) in stabilizing mutualisms, and the existence of “cheaters” (species gaining fitness by not benefiting their hosts) and their role in destabilizing them are controversial. A detailed study of an evolutionary transition from mutualism to parasitism focusing on two functionally distinct Eupristina wasp species associated with the fig, Ficus microcarpa in Yunnan Province, China, documents both. Within the comparative context of many existing studies of costs and benefits of active fig pollination, the results suggest that the low to nonexistent host sanctions on wasps that do not pollinate in this region promote the loss of specialized morphologies and behaviors crucial for pollination and, thereby, the evolution of cheating.