Soil salinity is a major stress limiting agricultural productivity worldwide. To counteract the adverse effects of salinity, plants from coastal habitats may engage in positive interaction with microbial partners. We recently discovered inland and coastal populations of Brassica fruticulosa with contrasting salinity tolerance. Here we characterize the microbiomes of salt-tolerant (PST) and salt-sensitive (PSS) populations, analyzing the diversity and abundance of bacteria and fungi taxa in bulk soil, rhizosphere, roots, and leaves of eight populations. We tested in a reciprocal transplant experiment the effects of two salt-tolerant (MST) and two salt-sensitive (MSS) rhizospheric microbiomes on PST and PSS plants under high salinity. Inoculation with MST enhanced salinity tolerance, improved growth, nutritional status, and reduced oxidative stress of PSS plants. Later, we isolated 113 bacterial strains from MST, 26 of which grew in 150mM NaCl and exhibited phosphate solubilization and siderophore production mechanisms. Further screening for nitrogen fixation, auxin production, and ACC deaminase activity allowed us to select 15 top candidates for mediating tolerance. Only five strains significantly promoted salt-sensitive plants growth under saline conditions. These findings highlight that the microbiome of species adapted to harsh conditions harbor a reservoir of potentially beneficial microorganisms that may improve plant resilience to salinity.