Although desert soils support functionally important microbial communities that affect plant growth and influence many biogeochemical processes, the impact of future changes in precipitation patterns on the microbiota and their activities is largely unknown. We performed in‐situ experiments to investigate the effect of simulated rainfall on bacterial communities associated with the widespread perennial shrub, Rhazya stricta in Arabian desert soils. The bacterial community composition was distinct between three different soil compartments: surface biological crust, root‐attached, and the broader rhizosphere. Simulated rainfall had no significant effect on the overall bacterial community composition, but some population‐level responses were observed, especially in soil crusts where Betaproteobacteria, Sphingobacteria, and Bacilli became more abundant. Bacterial biomass in the nutrient‐rich crust increased three‐fold one week after watering, whereas it did not change in the rhizosphere, despite its much higher water retention. These findings indicate that between rainfall events, desert‐soil microbial communities enter into stasis, with limited species turnover, and reactivate rapidly and relatively uniformly when water becomes available. However, microbiota in the crust, which was relatively enriched in nutrients and organic matter, were primarily water‐limited, compared with the rhizosphere microbiota that were co‐limited by nutrients and water.