Gut microbiomes are integral to animal eco-physiology and are hypothesized to shape the adaptive evolution of animal life. However, directly estimating the extent to which gut microbiomes are under selection within free-living animal populations is challenging. The inheritance mechanisms that allow for the intergenerational transmission of microbiome variation within animal populations are also unclear. However, joint characterization of the inheritance and fitness consequences of microbiome variation are critical for understanding the role of microbiota in animal adaptation. To address these knowledge gaps in parallel, I quantified relationships between gut microbiomes and host survival in the wild, by using shallow shotgun metagenomic sequencing to characterize microbiota communities in archived fecal samples collected across seven years of a long-term individual-based study of Sable Island feral horses (2820 samples from 905 individuals). Using quantitative genetic animal models, I then estimated the narrow-sense heritability and social transmissibility of survival-associated microbiota. Analysis of these data indicate that horse survival may be strongly connected to methane production in the hindgut. Furthermore, quantitative genetic analyses suggest the involvement of both host genetics and social effects in structuring the microbiome, and that these effects may be strongest for the microbiota most closely connected to horse survival. By dovetailing estimates of natural selection and inheritance, these results provide a fuller understanding of how host-microbiome relationships evolve in nature.