Ralstonia solanacearum, the causal agent of a lethal bacterial wilt disease, infects many plants that include an unusually wide range of susceptible hosts as well as tolerant (asymptomatic) hosts. The ability of this pathogen to adapt to many plants is also supported by field observations reporting emergence of strains with enlarged pathogenic properties. To investigate the genetic and epigenetic bases of host adaptation, we conducted evolution experiments by serial passages of a single clone of the pathogen on two susceptible and three tolerant plant species over 300 bacterial generations and then analyzed the genomes, transcriptomes and methylomes of 31 evolved clones. Phenotypic analysis of the evolved clones showed that the pathogen can increase its fitness both on susceptible and tolerant hosts although the magnitude of the adaptive process appeared more important on tolerant hosts. Genomic sequence analysis of evolved clones identified few genetic alterations but we provide evidence that most of them were adaptive mutations. Transcriptomic analyses revealed that even if different adaptive events occurred in independently evolved clones, there is convergence towards a global rewiring of the virulence regulatory network as evidenced by largely overlapping gene expression profiles. Significant transcriptomic variations were also detected in evolved clones showing no genomic polymorphism, suggesting that epigenetic modifications regulate expression of some of the virulence network components and play a major role in adaptation as well. To test this hypothesis, we investigated methylome variation in the evolved clones using SMRT-sequencing approach. This analysis revealed differential methylated regions (DMRs) at the GTWWAC motif in the evolved clones. Using site-directed mutagenesis, we demonstrated the contribution of one DMR in host adaptation. These data encourage future works to better understand the role of DNA methylation in the adaptive processes of R. solanacearum to a wide range of host species.