Marine-terrestrial transition represents an important aspect of organismal evolution that requires numerous morphological and genetic innovations and has been hypothesized to be caused by geological changes. We used talitrid crustaceans with marine-coastal-montane extant species at a global scale to investigate the marine origination and terrestrial adaptation. Using genomic data, we demonstrated that marine ancestors repeatedly colonized montane terrestrial habitats during the Oligocene to Miocene. Biological transitions were well correlated with plate collisions or volcanic island formation, and top-down cladogenesis was observed on the basis of a positive relationship between ancestral habitat elevation and divergence time for montane lineages. We detected convergent variations of convoluted gills and convergent evolution of SMC3 associated with montane transitions. Moreover, using CRISPR-Cas9 mutagenesis, we proposed that SMC3 potentially regulates the development of exites, such as talitrid gills. Our results provide a living model for understanding biological innovations and related genetic regulatory mechanisms associated with marine-terrestrial transitions.