The evolution of endosymbiont genomes is likely influenced by the ecological interactions with their hosts. Here, we studied the evolution of Spiroplasma genomes detected within Morpho butterflies sampled in the wild. Spiroplasma was detected in 4 out of the 11 Morpho species studied and displayed a 3 times larger genome size as compared to Spiroplasma genomes documented in other hosts. This inflation in genome size is caused by massive and recent expansion of various mobile genetic elements and by the acquisition of new genes stemming from prophages. In particular, we documented the peculiar evolution of the toxin genes in plasmids that may enhance host resistance to parasites. Phylogenetic comparisons with Spiroplasma extracted from other host point at a unique origin of Spiroplasma in Morpho, and strong divergence from Spiroplasma found in other Lepidoptera. Resequencing data obtained for multiple populations of the two sister-species M. helenor and M. achilles living in sympatry over the majority of their distribution revealed a opposite prevalence (97% in M. achilles and 3% in M. helenor), suggesting contrasted ecological interactions with these two host-species. Reconciliation analysis of the phylogenetic relationships of Morpho mitochondrial genomes and Spiroplasma genomes was then consistent with a predominant vertical transfer of the endosymbiont. Altogether, our results suggest a key role of ecological interactions with the host in the evolution of endosymbiont genomes and point at a putative interaction of Spiroplasma with reproductive isolation between sympatric species of butterflies.