Little is known about the effects of El Niño-Southern Oscillation (ENSO) on tropical insect communities, even though they are suffering rapid declines in complexity and stability due to climate change. We explore the impact of fluctuations in local climate imposed by ENSO on the performance of herbivore defences mediating enemy interactions. In a widespread rainforest edge community, we quantified the mortality caused by five enemy guilds on the immature stages of the herbivorous beetle, Acromis sparsa. ENSO was a significant determinant of beetle mortality. During warmer, drier El Niño years, the survival of beetles decreased. This was due to increased egg parasitism by wasps, which reduced hatching. Additionally, ant predation on beetle larvae increased. Flies and wasps were in competition for larval prey in wetter, cooler La Niña years. Experimental removal of maternal guards or chemical shields revealed which ENSO-related parameters predicted larval mortality. Guarding was most effective against social wasps in La Niña, whereas shields proved most effective in El Niño. Two ENSO-related defence–enemy breakdowns occurred: (1) decoupling whereby the efficacy of a narrow defensive adaptation was reduced to increase mortality, and (2) mismatching whereby the resistance of a narrow defensive adaptation against non-targeted enemies was further reduced to increase mortality. These results highlight that defence efficacy against natural enemies can vary predictably with biotic and abiotic environmental conditions. ENSO events will increase breakdowns in defence-mediated interactions, shifts in competition among enemies, and species loss.