Pantoea ananatis is an unusual bacterial necrotroph causing center rot of onion, a recurrent disease of concern in many onion producing regions. It is predicted to produce an, as of yet, unidentified phosphonate phytotoxin as a primary virulence factor to kill host plant cells. When damaged, onion and other alliaceous plants produce the characteristically pungent phytoanticipin allicin. Allicin is an antimicrobial reactive sulfur compound and oxidant that reacts spontaneously with thiol groups and depletes the reduced glutathione pool. We used comparative genomics of P. ananatis strains with variable pathogenicity on onion, to identify four clusters of plasmid-borne genes that strongly correlated with onion virulence. Among these, we found a sub-cluster of 11 contiguous genes enriched for annotated functions in sulfur metabolism and thiol redox homeostasis. We found that engineered deletions lacking these genes reached 100-fold lower populations in onion bulb scales. Natural variant Pantoea isolates and engineered mutant strains lacking these genes had major growth defects in red onion juice as well as increased sensitivity to garlic juice and purified allicin. In addition, a nearly identical cluster of plasmid-borne allicin tolerance genes was identified in a sequenced onion pathogenic Enterobacter cloacae strain. We hypothesize that the acquisition of allicin tolerance genes by horizontal gene transfer is a common strategy for pathogenic bacteria that aggressively colonize onion bulb tissue.