Assessing the heat tolerance (CTmax) of organisms is central to understand the impact of climate change on biodiversity. While both environment and evolutionary history affect CTmax, it remains unclear how these factors and their interplay influence ecological interactions, communities and ecosystems under climate change. We collected and reared caterpillars and parasitoids from canopy and ground layers in different seasons in a tropical rainforest. We tested the CTmax and Thermal Safety Margins (TSM) of these food webs with implications for how species interactions could shift under climate change. We identified strong influence of phylogeny in herbivore–parasitoid community heat tolerance. The TSM of all insects were narrower in the canopy and parasitoids had lower heat tolerance compared to their hosts. Our CTmax-based simulation showed higher herbivore–parasitoid food web instability under climate change than previously assumed, highlighting the vulnerability of parasitoids and related herbivore control in tropical rainforests, particularly in the forest canopy.