The Segatella copri (formerly Prevotella copri) complex (ScC) comprises taxa that are key members of the human gut microbiome. It was previously described to contain four distinct phylogenetic clades. Combining targeted isolation with large-scale metagenomic analysis, we defined 13 distinct Segatella copri-related species, expanding the ScC complex beyond four clades. Complete genome reconstruction of thirteen strains from seven species unveiled the presence of genetically diverse large circular extrachromosomal elements. These elements are consistently present in most ScC species, contributing to intra- and inter-species diversities. The nine species-level clades present in humans display striking differences in prevalence and intra-species genetic makeup across human populations. Based on a meta-analysis, we found reproducible associations between members of ScC and the male sex and positive correlations with lower visceral fat and favorable markers of cardiometabolic health. Our work uncovers genomic diversity within ScC, facilitating a better characterization of the human microbiome. Display omitted •Segatella copri (formerly Prevotella copri) complex includes 13 distinct species•Large extrachromosomal elements contribute to ScC intra- and inter-species diversities•ScC presents a genetic structure linked to geographic origin and lifestyle•ScC is associated with males, low visceral fat, and improved glucose responses Prevalent human gut commensal bacteria feature a hidden variability hampering molecular and clinical studies. Blanco-Míguez et al. utilize cultivation-dependent and cultivation-independent approaches to describe the Segatella copri complex (ScC). They identify that ScC members contain distinct genomic elements and content as well as display variable association to host phenotypes.