Plant-associated microorganisms are considered a key determinant of plant health and growth. However, little information is available regarding the composition and ecological function of the roots' and leaves' bacterial microbiota of halophytes. Here, using both culture-dependent and culture-independent techniques, we characterized the bacterial communities of the roots and leaves as well as the rhizosphere and bulk soils of the coastal halophyte in Jiangsu Province, China. We identified 49 representative bacterial strains belonging to 17 genera across all samples, with as the most dominant genus. All isolates showed multiple potential plant growth promotion traits and tolerated a high concentration of NaCl and a wide pH range. Interestingly, further inoculation experiments showed that the strain KLBMP 5180 isolated from root tissue significantly promoted host growth under NaCl stress. Indeed, KLBMP 5180 inoculation increased the concentrations of total chlorophyll, proline, antioxidative enzymes, flavonoids, K, and Ca in the leaves; the concentrations of malondialdehyde (MDA) and Na were reduced. A transcriptome analysis identified 1,359 and 328 differentially expressed genes (DEGs) in inoculated seedlings treated with 0 and 250 mM NaCl, respectively. We found that pathways related to phenylpropanoid and flavonoid biosynthesis and ion transport and metabolism might play more important roles in host salt stress tolerance induced by KLBMP 5180 inoculation compared to that in noninoculated leaves. Our results provide novel insights into the complex composition and function of the bacterial microbiota of the coastal halophyte and suggest that halophytes might recruit specific bacteria to enhance their tolerance of harsh environments. Halophytes are important coastal plants often used for the remediation of saline coastal soils. is well known for its medical properties and phytoremediation of saline soils. However, excessive exploitation and utilization have made the wild resource endangered. The use of endophytic and rhizosphere bacteria may be one of the suitable ways to solve the problem. This study was undertaken to develop approaches to improve the growth of using endophytes. The application of actinobacterial endophytes ameliorated salt stress damage of the host via complex physiological and molecular mechanisms. The results also highlight the potential of using habitat-adapted, symbiotic, indigenous endophytic bacteria to enhance the growth and ameliorate abiotic stress damage of host plants growing in special habitats.