Xanthomonas vasicola pv. vasculorum (Xvv) is an emerging bacterial plant pathogen that causes bacterial leaf streak on corn. First described in South Africa in 1949, reports of this pathogen have greatly increased in the past years in South America and in the U.S. The rapid spread of this disease in North and South America may be due to more favorable environmental conditions, susceptible hosts and/or genomic changes that favored the spread. To understand whether genetic mechanisms exist behind the recent spread of Xvv we used comparative genomics to identify gene acquisitions in Xvv genomes from the U.S. and Argentina. We sequenced 41 genomes of Xvv and the related sorghum-infecting X. vasicola pv. holcicola (Xvh), and performed comparative analyses against all available X. vasicola genomes. Time-measured phylogenetic analyses showed that Xvv strains from the U.S. and Argentina are closely related and arose from two introductions to North and South America. Gene content comparisons identified clusters of genes enriched in corn Xvv that showed evidence of horizontal transfer including one cluster corresponding to a prophage found in all Xvv strains from the U.S. and Argentina as well as in Xvh strains. In this work we explore the genomes of an emerging phytopathogen population as a first step towards identifying genetic changes associated to the emergence. The acquisitions identified may contain virulence determinants or other factors associated with the spread of Xvv in North and South America, and will be the subject of future work.