Rain-fed plants are subjected to cycles of drought and re-watering. Thus, efficient recovery from drought may be among the key determinants in the success of these plants. We performed a fine-scale time course of bulk RNA sequencing and revealed that transcriptional drought recovery is an active and rapid process involving activating over 3000 recovery-specific genes. Upon rehydration, we found a rapid microbial-autonomic induction of the immune system. We termed this response drought recovery-induced immunity (DRII). To reveal the immediate cell-type-specific responses to rehydration that initiates recovery, we performed a single-nucleus transcriptome analysis of plants recovering from long-term moderate drought and profiled >126,000 transcriptomes. We found that the DRII response manifests in sub-populations of epidermal and mesophyll cells immediately following rehydration. This response was also observed in an unidentified population of cells with a strong transcriptional immune activation signature. Finally, inoculation assays with Pseudomonas syringae pv. tomato DC3000 demonstrated that DRII increases plants’ pathogen resistance. To examine if DRII is a general phenomenon, we tested DRII in response to inoculation with two model pathogens in wild (Solanum pennellii) and domesticated (Solanum lycopersicum cv. M82) tomato. Our results indicated that short-term recovery from moderate drought could activate a preventive immune response in both Arabidopsis and tomato and reduce bacterial load in drought-recovered plants infected by pathogenic bacteria. Our results further indicate that DRII had maintained despite extensive selection during crop domestication as it exists in wild and cultivated tomato. Since rehydration increases microbial proliferation and, thus, the risk for infection, the DRII response may be crucial for plant survival in water-fluctuating environments.