Abstract Aim The halotolerant endophytic bacterial Pseudomonas strain EB3 isolated from the roots of the mangrove plant species Avicennia alba, has been reported to promote plant growth and mitigate the adverse effects of salt stress. However, the genetic mechanisms of the strain that may explain these processes are unknown. This study aimed to determine the whole genome sequence of EB3, and conduct expression analysis of EB3 genes putatively involved in salt tolerance and plant growth promotion. Methods and Results EB3-inoculated banana (Musa acuminata cv Berangan) plantlets were subjected to 100 mM sea salt. These inoculated plants exhibited significantly improved growth compared to non-inoculated controls under the same salinity stress. Whole-genome sequencing of EB3 revealed a genome size of 6 006 826 bp. Phylogenetic analysis based on whole-genome comparison indicated that EB3 is closely related to Pseudomonas juntendi. Functional annotation of the genome identified a large number of genes associated with key biological processes, including stress resistance, iron uptake system, plant root colonisation, and plant growth promotion. The increased expression of succinate-semialdehyde dehydrogenase (gabD), pyrroloquinoline quinone biosynthesis proteins (pqqBDEF), acetylglutamate kinase (argB), NADP-specific glutamate dehydrogenase (gdhA), N-acetylglutaminylglutamine synthetase (ngg), and superoxide dismutase family protein (sodC) genes in EB3, when EB3-inoculated plants were placed under salt stress, further supported their potential involvement in salt tolerance and growth-promoting activities. Conclusion Together, the genomic insights and gene expression data confirm the functional potential of the EB3 strain as a plant growth-promoting bacterium (PGPB) even under saline conditions.