Introduction: Priestia megaterium is noted as soil and plant microbe, with antimicrobial (Cui et al., 2023) and plant growth promotion (Bhatt et al., 2020) activities. Genomic analysis of endophytes, along with comparative genomics revealed potential genes linked to endophytism (Pinski et al., 2019). Goals: We aimed to assess potential genetic and physiological features employed by P. megaterium B1, isolated from apple roots, to adapt to the plant niche and enhance its growth. Also, we intended to explore genetic markers distinguishing plant-derived P. megaterium strains from soil ones, to deepen our understanding of possible traits influencing B1's plant association. Methods: We extensively analysed strain B1's genome, emphasizing genes tied to endophytism, and plant growth promotion. Validation through physiological tests was performed. Our genomic comparison included pan-genome and sparse partial least square discriminant (sPLS-DA) analyses, based on high quality genomes of 27 plant strains and 31 soil strains, beside strain B1. Functional enrichment of Pfam domains in both groups was done. Genes involved in plant-microbe interaction and plant growth promotion were explored for each strain. Results: Genomic analysis of B1 revealed putative genes related to motility and biofilm formation, confirmed by physiological tests. B1 showed genetic and physiological potential to produce indole-3-acetic acid and siderophores, and solubilize phosphate and zinc. The pan-genome analysis of 59 strains uncovered a close pan-genome. Strains from soil and plants displayed comparable genome sizes. SPLS-DA showed discriminative clustering, but functional enrichment analysis did not reveal significant enrichment of Pfam domains in either habitats. Also genetic elements associated with endophytism and plant growth promotion were present in strains from both habitats. Summary: B1 possesses physiological and genomic potential to adapt to plant niche and promote its growth. Comparative genomic analysis implied a conserved genetic structure for potential endophytism among strains from both habitats, suggesting a possible transition between free-living and host-associated lifestyles.