Background <p>Drought critically compromises agricultural productivity and threatens sustainable wheat production. <i>Streptomyces pactum</i> Act12 confers benefits to plant growth under drought stress, but its possible effects on root-associated microbiomes remain understudied. Here, shotgun metagenome sequencing and culture-dependent approaches were integrated to investigate the responses of rhizosphere and rhizoplane microbiomes in dryland winter wheat to exogenous <i>S. pactum</i> Act12 and their potential linkage to plant drought resistance.</p> Results <p>Seed biopriming with <i>S. pactum</i> Act12 increased plant aboveground dry weight at flowering (by 63.2%) and maturation (by 41.9%) stages, leading to improved grain yield (by 8.7%). Microbial inoculation reduced malondialdehyde contents in wheat leaves and roots at the flowering stage alongside compartment-specific alterations in soil microbiomes. Metagenomic analysis revealed inoculation-induced enrichment of distinct taxa in rhizosphere soils (flowering: Fibrobacterota, <i>Altererythrobacter</i>; maturation: Mucoromycota, <i>Rhodospirillum</i>) and rhizoplane soils (flowering: Pseudomonadota, <i>Serratia</i>; maturation: Candidatus_Pacebacteria, <i>Variovorax</i>). Functional profiling showed up-regulation of key pathways related to oxidative phosphorylation in inoculated rhizosphere soils at the flowering stage. In rhizoplane soils, ABC transporters and pyrimidine metabolism were up-regulated across stages upon inoculation. Two key strains isolated from rhizoplane soils, designated <i>Glycomyces lechevalierae</i> A4 and <i>Microbacterium algeriense</i> B3, demonstrated the ability to enhance drought resistance in wheat seedlings.</p> Conclusions <p>Inoculation of <i>S. pactum</i> Act12 heightens drought resistance in dryland winter wheat through compartment-specific phylogenetic restructuring and functional reprogramming of root-associated microbiomes.</p>