Genus Xanthomonas is a group of phytopathogens that is phylogenetically related to Xylella, Stenotrophomonas, and Pseudoxanthomonas, having diverse lifestyles. Xylella is a lethal plant pathogen with a highly reduced genome, atypical GC content and is taxonomically related to these three genera. Deep phylo-taxono genomics reveals that Xylella is a variant Xanthomonas lineage that is sandwiched between Xanthomonas clades. Comparative studies suggest the role of unique pigment and exopolysaccharide gene clusters in the emergence of Xanthomonas and Xylella clades. Pan-genome analysis identified a set of unique genes associated with sub-lineages representing plant-associated Xanthomonas clade and nosocomial origin Stenotrophomonas clade. Overall, our study reveals the importance of reconciling classical phenotypic data and genomic findings in reconstituting the taxonomic status of these four genera. SIGNIFICANCE STATEMENT: Xylella fastidiosa is a devastating pathogen of perennial dicots such as grapes, citrus, coffee, and olives. An insect vector transmits the pathogen to its specific host wherein the infection leads to complete wilting of the plants. The genome of X. fastidiosa is significantly reduced both in terms of size (2 Mb) and GC content (50%) when compared with its relatives such as Xanthomonas, Stenotrophomonas, and Pseudoxanthomonas that have higher GC content (65%) and larger genomes (5 Mb). In this study, using systematic and in-depth genome-based taxonomic and phylogenetic criteria and comparative studies, we assert the need to unify Xanthomonas with its relatives (Xylella, Stenotrophomonas and Pseudoxanthomonas). Interestingly, Xylella revealed itself as a minor variant lineage embedded within two major Xanthomonas lineages comprising member species of different hosts.