Salinity is challenging agriculture by reducing crop productivity. Endophytes from halophyte plants have the potential to alleviate salinity stress in crops. Here, 78 bacterial strains were recovered from 10 habitat-adapted halophyte plants in the central deserts of Iran. Eight superior halotolerant strains tolerating 3 M NaCl, were identified as the Gram-positive genera Bacillus and Oceanobacillus (Bacillaceae), Brachybacterium (Dermabacteraceae), Micrococcus (Micrococcaceae), and Salinicoccus (Staphylococcaceae). Scanning electron microscopy (SEM) showed that the most halotolerant strain, i.e., Salinicoccus hispanicus, experienced accelerated binary fission under salinity. Furthermore, seeds of the two winter wheat cultivars, i.e., cv. Homa (rain-fed) and cv. Mihan (irrigated), inoculated by those bacteria, showed enhanced germination indices under different salinity gradients, and also under normal conditions. Indeed, the superior bacteria, i.e., Oceanobacillus sp. strain 76, Micrococcus luteus strain 14, and Bacillus sp. strain 7, enhanced seed germination indices in both wheat cultivars including final seed germinations, as well as the root, shoot and seedling lengths. These strains were capable of producing the plant hormone auxin (IAA). Thus, we propose that halotolerant endophytic bacteria from desert-adapted halophyte plants could alleviate salinity stress in strategic crops such as the wheat Triticum aestivum L., especially in dryland farming.