Wolbachia pipientis is an intracellular endosymbiotic bacterium that blocks replication of several arboviruses in transinfected Aedes aegypti mosquitoes. However, the Wolbachia-mediated antiviral mechanism remains largely unknown. We explored the effect of Wolbachia on the expression of the host m6A machinery and if the post-transcriptional modification landscape is altered in the presence of Wolbachia by direct RNA sequencing using the nanopore technology. Mosquito METTL3 and m6A machinery/m6A methyltransferase complex gene expression was elevated in Wolbachia-transinfected cells. Knocking down host m6A-writers, -reader, and -eraser genes using double stranded RNA had no effect on Wolbachia density. Nanopore direct RNA sequencing of wAlbB strain of Wolbachia and Wolbachia-free Aag2 cells showed almost double the number of differentially modified N6-methyladenosine (m6A) sites on mosquito transcripts in Wolbachia colonised cells. m6A in Ae. aegypti were especially enriched within the coding sequence and 3′-untranslated regions. Differential gene expression analysis revealed a critical host factor, transmembrane protein 41B (TMEM41B) required for flavivirus infection upregulated by several fold-change magnitudes. Several classical and non-classical immune-related genes were amongst the downregulated DEG’s. Our findings demonstrate Wolbachia’s ability to alter many intracellular aspects of its host by influencing post-transcriptional m6A modifications and gene expression.