Human agriculture has always raced against insect adaptation, requiring updated pest control methods and knowledge of evolutionary processes. Excessive exposure to blue light (BL) kills a wide range of insect species and has attracted attention as an alternative to chemical pesticides. Here, to understand how insects adapt to BL toxicity, we investigated evolutionary responses to BL toxicity in Drosophila melanogaster over 70 generations using laboratory selection experiments. The selected line exhibited an obese phenotype accompanied by midgut elongation, with BL tolerance dependent on gut microbiota-mediated lipid accumulation. Whole-genome and transcriptome analyses consistently highlighted interactions between the microbiota and host lipid metabolism-related genes. Remarkably, manipulating genes associated with lipid accumulation conferred BL tolerance even in the absence of selection. We suggest that the acquisition of BL tolerance occurs through 'adaptive obesity'. Our study introduces a mechanism of evolutionary adaptation of insects against BL-based selective pressure by maximising the benefits from the gut microbiota via midgut elongation.