Shifts in the soil microbiome during continuous monoculture cropping coincide with increased suppressiveness against soil-borne diseases, as in the take-all decline of wheat. Here we report a similar phenomenon for bacterial blotch of mushrooms, caused by Pseudomonas ‘gingeri’, where ginger blotch incidence decreases during consecutive cycles of mushroom cultivation. We explored the infection dynamics of blotch during consecutive cultivation cycles for different casing soil mixtures. We also observed the population dynamics of the pathogen in these casing soils. In addition, the composition of the casing soil microbiome was compared between blotch suppressive and conducive soils. Finally, we studied the transferability of blotch suppressiveness. A consistent decline of bacterial blotch was observed for two consecutive cultivation cycles of mushroom cropping, across ten casing soil mixtures composed of different peat sources and supplements. Blotch suppression occurred without reduction of pathogen populations in the casing soils. Aqueous extracts made from suppressive soils were able to reduce blotch incidence in conducive casing soils, indicating that blotch suppression is transferrable and microbially mediated. Changes in the microbial community composition of the casing soils reflected pathogen invasion, pathogen establishment and disease suppression, in addition to the expected temporal changes across the cultivation cycles. Specific bacterial genera were associated with soil suppressiveness to bacterial blotch, such as, Pseudomonas sp., Dyadobacter sp., Pedobacter sp., and Flavobacterium sp. We suggest that the suppression of bacterial blotch is induced due to high pathogen populations in the first cultivation cycle, and mediated by inhibition of virulence factors such as those controlled by quorum sensing in the later cultivation cycles.