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Salt stress is a serious agricultural problem threatens plant growth and development resulted in productivity loss and global food security concerns. Salt tolerant plant growth promoting actinobacteria, especially deep-sea actinobacteria are an alternative strategy to mitigate deleterious effects of salt stress. In this study, we aimed to investigate the potential of deep-sea <i>Dermacoccus abyssi</i> MT1.1^T to mitigate salt stress in tomato seedlings and identified genes related to plant growth promotion and salt stress mitigation. <i>D. abyssi</i> MT1.1^T exhibited plant growth promoting traits namely indole-3-acetic acid (IAA) and siderophore production and phosphate solubilization under 0, 150, 300, and 450 mM NaCl in vitro. Inoculation of <i>D. abyssi</i> MT1.1^T improved tomato seedlings growth in terms of shoot length and dry weight compared with non-inoculated seedlings under 150 mM NaCl. In addition, increased total soluble sugar and total chlorophyll content and decreased hydrogen peroxide content were observed in tomato inoculated with <i>D. abyssi</i> MT1.1^T. These results suggested that this strain mitigated salt stress in tomatoes via osmoregulation by accumulation of soluble sugars and H₂O₂ scavenging activity. Genome analysis data supported plant growth promoting and salt stress mitigation potential of <i>D. abyssi</i> MT1.1^T. Survival and colonization of <i>D. abyssi</i> MT1.1^T were observed in roots of inoculated tomato seedlings. Biosafety testing on <i>D. abyssi</i> MT1.1^T and in silico analysis of its whole genome sequence revealed no evidence of its pathogenicity. Our results demonstrate the potential of deep-sea <i>D. abyssi</i> MT1.1^T to mitigate salt stress in tomato seedlings and as a candidate of eco-friendly bio-inoculants for sustainable agriculture.