Pathogenic microbes cause systemic and non-systemic diseases of plant and animal hosts. Systemic diseases are particularly destructive because the pathogen moves through the host vasculature causing widespread infection; meanwhile non-systemic pathogens remain restricted to the nonvascular tissue near the site of infection. The basis of systemic and non-systemic pathogenesis is unclear. Here we describe the role of cell wall degradation in the evolution and biology in the Gramnegative phytobacterial genus Xanthomonas. Xanthomonas comprises a diverse group of vascular and non-vascular pathogens of over 200 plant species. We demonstrate that a single, vascular pathogen-unique cell wall degrading enzyme called CelA contributes to systemic pathogenesis in multiple pathogenic lineages in this diverse genus. We determined that CelA1 was conserved only in systemic pathogenic bacteria in the genera Xanthomonas, Xylella and Ralstonia but absent in nonsystemic Gram-negative plant pathogenic bacteria. Most notably addition of this cell wall degrading enzyme to two distinct non-systemic pathogen species, barley-infecting Xanthomonas translucens and rice-infecting Xanthomonas oryzae, permitted systemic pathogenesis of their respective host plants. Further genomic analysis of non-systemic Xanthomonas pathogens appear to have inactivated this trait suggesting that they arose from related vascular subgroups upon adapting to the non-vascular plant environment. Overall this work provides a framework to describe pathogen emergence based on symptom development and tissue-specificity in an important pathogen genus.