Pantoea ananatis is a significant bacterial pathogen responsible for onion center rot (OCR) in bulb onions (Allium cepa). The pathogen’s virulence in onions is attributed to two major genetic systems: the chromosomal HiVir cluster and the plasmid-borne allicin tolerance (alt) gene cluster, which allow the bacterium to overcome onion-derived antimicrobial thiosulfinates and promote disease progression. However, the genetic factors involved in infecting non-bulb Allium species like the leeks (A. porrum), Welsh onions (A. fistulosum), and chives (A. schoenoprasum) remain poorly understood, leading to an incomplete understanding of the PA-Allium pathosystem. In our initial objective 92 P. ananatis strains were screened for pathogenicity on A. fistulosum × A. cepa and A. porrum. Our results revealed higher aggressiveness on the hybrid species, while genome-wide association studies (GWAS) identified 835 genes linked to pathogenicity on A. fistulosum × A. cepa and 243 genes associated with infection on A. porrum. This suggests that P. ananatis may utilize a shared set of virulence genes for Allium infection but requires host-specific adaptations for non-bulb species. We further validated that the HiVir gene cluster is the primary pathogenicity factor across A. cepa, A fistulosum, and A. porrum. To explore thiosulfinate tolerance, we employed Natural Language Processing (NLP)-like deep learning techniques to identify alt-like gene clusters across 238,362 bacterial genomes. The model discovered 47 novel alt-like clusters, 15 of which we experimentally validated in PA strains, showing enhanced tolerance in onion extract assays. This highlights the utility of deep learning in uncovering diverse gene clusters that might otherwise remain hidden, and by extension, enabling a greater capacity to investigate PA-Allium interactions. Finally, we screened 982 Allium genotypes and identified a resistant A. cepa genotype, DPLD 19-39, which consistently exhibited reduced necrosis and bulb rot. Transcriptomic analysis indicated that resistance is mediated by cell wall fortification, reactive oxygen species (ROS) regulation, and programmed cell death. These defense mechanisms provide key targets for breeding programs aimed at developing PA-resistant onion cultivars, offering a promising path for mitigating crop losses and improving agricultural sustainability.