Members of the classOpitutaeare widely distributed in various environments such as rice paddy soil, freshwater lakes, seawater, marine sediment, and invertebrate digestive tracts. The class currently consists of two orders,OpitutalesandPuniceicoccales, represented by the familiesOpitutaceaeandPuniceicoccaceae, respectively, which are primarily delineated on the basis of 16S rRNA gene sequences and limited phenotypic characterizations of a few type strains. The scarcity of 16S rRNA gene and genome sequences generated from the type strains of the classOpitutaeconstrained our understanding of the ecological distribution and adequate resolution of its taxonomy. Here, anOpitutaestrain designated WMMB3T, isolated from a mangrove sediment, was subjected to taxonomic characterization. The 16S rRNA gene of strain WMMB3Tshared high sequence similarities withCoraliomargarita akajimensisDSM 45221TandC. sinensisWN38Tof 96.1 and 95.9%, respectively. Phylogenetic analysis suggested that strain WMMB3Tformed a monophyletic branch affiliated to the genusCoraliomargarita. The average nucleotide identity (ANI) values, digital DNA–DNA hybridization (dDDH) values and average amino acid identity (AAI) values of strain WMMB3Tcompared betweenCoraliomargaritamembers were 71.8–72.5, 20.7, and 68.2–68.7%, respectively, indicating that strain WMMB3Trepresented a novel species ofCoraliomargarita. The genome of strain WMMB3Twas 4.5 Mbp with a DNA G + C content of 56.0%. The respiratory quinone was menaquinone-7. The major fatty acids were iso-C14:0, and C18:1ω9c. Based on genomic, phenotypic, and chemotaxonomic characterizations, strain WMMB3Trepresents a novel species, andCoraliomargarita parvasp. nov. is proposed. Additionally, the phylogenomic analysis of more than 500 genomes of the classOpitutae, encompassing a majority of uncultivated bacteria and a few type strains, was performed using the Genome Taxonomic Database toolkit (GTDB-Tk) to present adequate resolution of the taxonomy. Combined with 16S rRNA gene sequence phylogeny and genomic relatedness, five novel families retrieved mainly from marine habitats were proposed:Coraliomargaritaceaefam. nov.,Pelagicoccaceaefam. nov.,Cerasicoccaeaefam. nov.,Oceanipulchritudinaceaefam. nov., andAlterococcaeaefam. nov. AAI values of 58–60% could be considered as the boundary to delineate families of the classOpitutae. This study provided a new taxonomic framework of the classOpitutaebased on the genomic data.