Salinity is an escalating agricultural challenge, yet plant microbiomes offer a promising avenue for improving salt tolerance. Nevertheless, most naturally occurring microbes remain unevaluated for plant growth–promoting function, and systematic approaches to uncover salt-tolerance-enhancing plant growth–promoting rhizobacteria (PGPR) are limited. Here, using soybean as a model, we implement a quantitative framework to characterize rhizosphere microbial networks and nominate novel taxa functionally associated with plant salt tolerance. We introduced a salt tolerance index (STI) to quantify plant salt tolerance and normalize performance across heterogeneous natural soil salinity. Metagenomic sequencing and co-occurrence analysis revealed distinct rhizosphere microbiota structures between tolerant and susceptible soybeans. In tolerant soybeans, Pseudomonas dominated as the hub of a highly interconnected network, whereas susceptible accessions showed a fragmented network dominated by Acinetobacter. Correlation analyses identified bacterial taxa positively associated with STI, including documented salt-tolerant PGPR and novel candidates. Greenhouse experiments showed that one candidate, Thalassospira xiamenensis, enhances soybean salt tolerance and reshapes host ion-transport and oxidative-stress gene expression under salinity, validating our screening strategy. Our culture-independent metagenomic association approach reveals host genotype–structured rhizosphere microbial networks underlying salt tolerance and provides an efficient, labor-saving means for high-throughput identification of salt-tolerant PGPR.