<jats:title>Abstract</jats:title><jats:p>Ecological differentiation between strains of bacterial species is shaped by genomic and metabolic variability. However, connecting genotypes to ecological niches remains a major challenge. Here, we linked bacterial geno- and phenotypes by contextualizing pangenomic, exometabolomic and physiological evidence in twelve strains of the marine bacterium <jats:italic>Alteromonas macleodii</jats:italic>, illuminating adaptive strategies of carbon metabolism, microbial interactions, cellular communication and iron acquisition. In <jats:italic>A. macleodii</jats:italic> strain MIT1002, secretion of amino acids and the unique capacity for phenol degradation may promote associations with <jats:italic>Prochlorococcus</jats:italic> cyanobacteria. Strain 83-1 and three novel Pacific isolates, featuring clonal genomes despite originating from distant locations, have profound abilities for algal polysaccharide utilization but without detrimental implications for <jats:italic>Ecklonia</jats:italic> macroalgae. Degradation of toluene and xylene, mediated via a plasmid syntenic to terrestrial <jats:italic>Pseudomonas</jats:italic>, was unique to strain EZ55. Benzoate degradation by strain EC673 related to a chromosomal gene cluster shared with the plasmid of <jats:italic>A. mediterranea</jats:italic> EC615, underlining that mobile genetic elements drive adaptations. Furthermore, we revealed strain-specific production of siderophores and homoserine lactones, with implications for nutrient acquisition and cellular communication. Phenotypic variability corresponded to different competitiveness in co-culture and geographic distribution, indicating linkages between intraspecific diversity, microbial interactions and biogeography. The finding of “ecological microdiversity” helps understanding the widespread occurrence of <jats:italic>A. macleodii</jats:italic> and contributes to the interpretation of bacterial niche specialization, population ecology and biogeochemical roles.</jats:p>