The taxonomy of marine and non-marine organisms rarely overlap, but the mechanisms underlying this distinction are often unknown. Here, we predicted three major ocean-to-land transitions in the evolutionary history of Flavobacteriaceae, a family known for polysaccharide and peptide degradation. These unidirectional transitions were associated with repeated losses of marine signature genes and repeated gains of non-marine adaptive genes. This included various Na+-dependent transporters, osmolyte transporters and glycoside hydrolases (GH) for sulfated polysaccharide utilization in marine descendants, and in non-marine descendants genes for utilizing the land plant material pectin and genes facilitating terrestrial host interactions. The K+ scavenging ATPase was repeatedly gained whereas the corresponding low-affinity transporter repeatedly lost upon transitions, reflecting K+ ions are less available to non-marine bacteria. Strikingly, the central metabolism Na+-translocating NADH: quinone dehydrogenase gene was repeatedly gained in marine descendants, whereas the H+-translocating counterpart was repeatedly gained in non-marine lineages. Furthermore, GH genes were depleted in isolates colonizing animal hosts but abundant in bacteria inhabiting other non-marine niches; thus relative abundances of GH versus peptidase genes among Flavobacteriaceae lineages were inconsistent with the marine versus non-marine dichotomy. We suggest that phylogenomic analyses can cast novel light on mechanisms explaining the distribution and ecology of key microbiome components.