ABSTRACT The class Hexacorallia, encompassing stony corals and sea anemones, plays a critical role in marine ecosystems. Coral bleaching, the disruption of the symbiosis between stony corals and zooxanthellate algae, is driven by seawater warming and further exacerbated by pathogenic microbes. However, how pathogens, especially viruses, contribute to accelerated bleaching remains poorly understood. Here the model sea anemone Nematostella vectensis is used to explore these dynamics by creating a transgenic line with a reporter gene regulated by sequences from two RIG‐I‐like receptor genes involved in antiviral responses. Under heat stress, the reporter genes showed significant upregulation. Further, transcriptomes from N. vectensis , Exaiptasia diaphana and the stony coral Stylophora pistillata were analysed to reveal stress‐induced activation of a set of bona fide immune‐related genes conserved between the three species. Population‐specific differences in stress‐induced transcriptional responses of immune‐related genes were evident in both Nematostella and Stylophora , depending on geographic origin. In Exaiptasia , the presence of zooxanthellae also influenced stress‐induced immune gene expression. To test whether the viruses themselves contribute to this immune response under stress, we subjected N. vectensis to heat stress and measured the transcription dynamics of resident viruses as well as selected antiviral genes. While the antiviral genes responded within hours of heat stress, viral gene expression was already upregulated within 30 min, suggesting that their increase might be contributing to the elevated immune response under stress, and consequentially, the further demise of organismal homeostasis. These findings highlight the interplay between environmental stress, viruses, immune responses and symbiotic states in Hexacorallia.