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Bacterial diseases of the edible white button mushroom <i>Agaricus bisporus</i> caused by <i>Pseudomonas</i> species cause a reduction in crop yield, resulting in considerable economic loss. We examined bacterial pathogens of mushrooms and bacteriophages that target them to understand the disease and opportunities for control. The <i>Pseudomonas</i><i>tolaasii</i> genome encoded a single type III protein secretion system (T3SS), but contained the largest number of non-ribosomal peptide synthase (NRPS) genes, multimodular enzymes that can play a role in pathogenicity, including a putative tolaasin-producing gene cluster, a toxin causing blotch disease symptom. However, <i>Pseudomonas</i><i>agarici</i> encoded the lowest number of NRPS and three putative T3SS while non-pathogenic <i>Pseudomonas</i> sp. NS1 had intermediate numbers. Potential bacteriophage resistance mechanisms were identified in all three strains, but only <i>P. agarici</i> NCPPB 2472 was observed to have a single Type I-F CRISPR/Cas system predicted to be involved in phage resistance. Three novel bacteriophages, NV1, ϕNV3, and NV6, were isolated from environmental samples. Bacteriophage NV1 and ϕNV3 had a narrow host range for specific mushroom pathogens, whereas phage NV6 was able to infect both mushroom pathogens. ϕNV3 and NV6 genomes were almost identical and differentiated within their T7-like tail fiber protein, indicating this is likely the major host specificity determinant. Our findings provide the foundations for future comparative analyses to study mushroom disease and phage resistance.