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Root−associated microbial communities play important roles in the process of adaptation of plant hosts to environment stressors, and in this perspective, the microbiome of halophytes represents a valuable model for understanding the contribution of microorganisms to plant tolerance to salt. Although considered as the most promising halophyte candidate to crop cultivation, Salicornia ramosissima is one of the least-studied species in terms of microbiome composition and the effect of sediment properties on the diversity of plant-growth promoting bacteria associated with the roots. In this work, we aimed at isolating and characterizing halotolerant bacteria associated with the rhizosphere and root tissues of S. ramosissima, envisaging their application in saline agriculture. Endophytic and rhizosphere bacteria were isolated from wild and crop cultivated plants, growing in different estuarine conditions. Isolates were identified based on 16S rRNA sequences and screened for plant-growth promotion traits. The subsets of isolates from different sampling sites were very different in terms of composition but consistent in terms of the plant-growth promoting traits represented. Bacillus was the most represented genus and expressed the wider range of extracellular enzymatic activities. Halotolerant strains of Salinicola, Pseudomonas, Oceanobacillus, Halomonas, Providencia, Bacillus, Psychrobacter and Brevibacterium also exhibited several plant-growth promotion traits (e.g., 3-indole acetic acid (IAA), 1-aminocyclopropane-1-carboxylic acid (ACC) deaminase, siderophores, phosphate solubilization). Considering the taxonomic diversity and the plant-growth promotion potential of the isolates, the collection represents a valuable resource that can be used to optimize the crop cultivation of Salicornia under different environmental conditions and for the attenuation of salt stress in non-halophytes, considering the global threat of arable soil salinization.