Nonnative plant infestations provide unique opportunities to investigate pathogen emergence with evolutionarily recent plant introduction events. The widespread distribution of invasive plants and their proximity to genetically related crops highlights the risks of nonnative plants acting as ancillary hosts and fostering microbial recombination and pathogen selection. Garlic mustard (Alliaria petiolata) is a widespread, nonnative cruciferous weed that grows throughout North America and along the forested edges of diverse agricultural fields. The recent identification of a novel Xanthomonas campestris pv. incanae strain isolated from a diseased A. petiolata population led to the current investigation of the distribution and diversity of X. campestris isolates from naturally infected A. petiolata. A total of 14 diseased A. petiolata sites were sampled across three states, leading to the identification of diverse X. campestris pathotypes and genotypes. Pathogenicity assays and multilocus sequence analyses identified pathogenic X. c. pv. incanae and X. c. pv. barbareae strains collected from disparate A. petiolata populations. Moreover, independently collected X. c. pv. incanae strains demonstrated a broad cruciferous host range by infecting cabbage (Brassica oleracea var. capitata), garden stock (Matthiola incana), and the cover crop yellow mustard (Guillenia flavescens). This study highlights the genetic variability and host potential of natural X. campestris populations and the potential risks to Brassica crops via widespread, dense garlic mustard reservoirs.