Although mutualisms are ubiquitous in nature, our understanding of the potential impacts of climate change on these important ecological interactions is deficient. Here, we report on a thermal stress-related shift from cooperation to antagonism between members of a mutualistic coral-dwelling community. Increased mortality of coral-defending crustacean symbionts Trapezia cymodoce (coral crab) and Alpheus lottini (snapping shrimp) was observed in response to experimentally elevated temperatures and reduced coral-host (Pocillopora damicornis) condition. However, strong differential numerical effects occurred among crustaceans as a function of species and sex, with shrimp (75%), and female crabs (55%), exhibiting the fastest and greatest declines in numbers. These declines were due to forceful eviction from the coral-host by male crabs. Furthermore, surviving female crabs were impacted by a dramatic decline (85%) in egg production, which could have deleterious consequences for population sustainability. Our results suggest that elevated temperature switches the fundamental nature of this interaction from cooperation to competition, leading to asymmetrical effects on species and/or sexes. Our study illustrates the importance of evaluating not only individual responses to climate change, but also potentially fragile interactions within and among susceptible species.