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Abstract Background piRNAs have a constitutive role in genome defence by silencing transposable elements in the germline. In the nematode Caenorhabditis elegans, piRNAs also induce epigenetic silencing of transgenes, which can be maintained for many generations in the absence of the piRNA pathway. The role of multi-generational epigenetic inheritance in adaptation to the environment is unknown. Results Here, we show that piRNA biogenesis is downregulated in response to a small increase in temperature. Some effects on gene expression persist into subsequent generations and are associated with a negative fitness cost. We show that simultaneous infection with pathogenic bacteria suppresses downregulation of the piRNA pathway in response to increased temperature. This effect is associated with increased fitness of progeny of infected animals in subsequent generations. Conclusions Our results show that the piRNA pathway integrates inputs from the environment to establish intergenerational responses to environmental conditions, with important consequences for the fitness of the subsequent generation.