The vertebrate lineage diverged into chondrichthyes (sharks, rays, and chimeras) and osteichthyes fishes approximately 420 mya, accumulating vast differences in their anatomy including the skin surface structure. The skin surface is the largest organ of the body, protecting eukaryotes from the external environment, and supporting diverse microscopic organisms. The fundamental processes which govern the diversity of the skin surface microbiome is expected to vary across the two lineages of fish, but this remains an outstanding question in science. Here we use whole shotgun metagenomics to test the phylosymbotic theory in the marine environment and describe the partitioning of microbiome diversity on the skin of four elasmobranchs and five teleost fish species to determine if skin surface features influence the distribution of microbiome diversity. First, we found that taxonomic and phylogenetic composition were correlated across microbiomes (Rho = 0.79), however each was only weakly correlated with gene function composition (Phylo-Func: Rho = 0.27; Taxa-Func: Rho = 0.24). Second, we found that the taxonomic and functional composition of the microbiomes where lineage specific, however do not follow a phylosymbiotic trend. Some elasmobranch species are more similar to a fish species than other elasmobranchs. Third, we show that elasmobranchs have lower taxonomic and phylogenetic α-diversity (p < 0.05) of their microbiome, compared with teleost fishes, while functional diversity is maintained across lineages. Last, the partitioning of the microbial diversity differed between elasmobranchs and teleost fish. We show that most diversity with each community dimension is found across individual replicates for both lineages, however sharks have more species-specific diversity than teleost. For gene functions, shark species switching, sharing more diversity than teleost fishes. Our results suggest elasmobranchs have a strong selective influence on the gene function diversity relative to teleost fishes. The findings of lower α taxonomic and phylogenetic diversity and greater gene function similarities among elasmobranchs relative to teleost fishes suggest that a lower subset of microbial species can reside at the skin interface microbiome, with specific functions necessary to reside in this niche. Our results support the hypothesis that shark skin is a unique surface where differing fundamental assemblage rules are interacting to shape the microbiome present.