Our view of host-associated microbiota remains incomplete due to the presence of as yet uncultured constituents. The Bacteroidales family S24-7 is a prominent example of one of these groups. Marker gene surveys indicate that members of this family are highly localized to the gastrointestinal tracts of homeothermic animals, and are increasingly being recognized as a numerically predominant member of the gut microbiota, however little is known about the nature of their interactions with the host. We have undertaken the first whole genome exploration of this family using 30 population genomes extracted from fecal samples of four different animal hosts: human, mouse, koala and guinea pig. We infer the core metabolism to be that of fermentative or nanaerobic bacteria, resembling that of related Bacteroidales families. In addition, we describe three trophic guilds within the family, plant glycan (hemicellulose and pectin), host glycan and α-glucan, each broadly defined by increased abundance of enzymes involved in the degradation of particular carbohydrates. The presence of trophic guilds within the family indicates the potential for niche partitioning and therefore specific roles for each guild in gut health and dysbiosis. We have observed fluctuations in the abundance of certain members of the family in association with increased susceptibility to graft-versus-host disease following transplant in the mouse model, the genomes of which are currently under investigation. As S24-7 representatives constitute a substantial component of the murine gut microbiota, as well as being present within the human gut, it is important that we continue to investigate the nature of their residency.