| Summary: | Abstract Many species interactions are dependent on environmental context, yet the benefits of obligate, mutualistic microbial symbioses to their hosts are typically assumed to be universal across environments. We directly tested this assumption, focusing on the symbiosis between the sap‐feeding insect Megacopta cribraria and its primary bacterial symbiont Candidatus Ishikawaella capsulata. We assessed host development time, survival, and body size in the presence and absence of the symbiont on two alternative host plants and in the insects' new invasive range. We found that association with the symbiont was critical for host survival to adulthood when reared on either host plant, with few individuals surviving in the absence of symbiosis. Developmental differences between hosts with and without microbial symbionts, however, were mediated by the host plants on which the insects were reared. Our results support the hypothesis that benefits associated with this host–microbe interaction are environmentally contingent, though given that few individuals survive to adulthood without their symbionts, this may have minimal impact on ecological dynamics and current evolutionary trajectories of these partners. OPEN RESEARCH BADGES This article has earned an Open Data Badge for making publicly available the digitally‐shareable data necessary to reproduce the reported results. The data is available at https://doi.org/10.5061/dryad.kg4bc56
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