Wolbachia, a widespread endosymbiotic bacterium, profoundly impacts insect hosts by distorting reproduction and population dynamics. Despite extensive laboratory research, its long-term effects on host evolution in nature remain poorly understood, especially the genomic consequences linked to disruptions in sex determination and reproductive processes. We present the first telomere-to-telomere (T2T) genome assembly of the sawfly Analcellicampa danfengensis and the complete genome of its symbiotic Wolbachia. Comparative population genomics across six Analcellicampa species revealed that Wolbachia-infected populations show starkly different demographic signals. While uninfected populations show similar demographic signals for both sexes, infected populations exhibit a lower apparent effective population size (Ne) in males, which may reflect a recurrent male bottleneck effect driven by Wolbachia-induced male scarcity. Genomic scans identified positively selected genes associated with reproductive functions, sensory perception, neural development, and longevity, suggesting that Wolbachia likely manipulates critical host pathways to promote its transmission. These findings provide direct genomic insights into Wolbachia as an evolutionary force, highlighting specific host genes and regions under selection resulting from these altered evolutionary dynamics. This work provides deeper insights into host-endosymbiont coevolution and has important implications for evolutionary theory and pest management strategies.