Phylosymbiosis was recently proposed to describe the eco-evolutionary pattern whereby the ecological relatedness of host-associated microbial communities parallels the phylogeny of related host species. Here, we analyze the prevalence of phylosymbiosis and its functional significance under highly controlled conditions by characterizing the microbiota of 24 animal species from four different groups (Peromyscus deer mice, Drosophila flies, mosquitoes, Nasonia wasps) and re-evaluate the phylosymbiotic relationships of seven species of wild hominids. We demonstrate three key findings. First, intraspecific microbiota variation is consistently less than interspecific microbiota variation, and microbiota-based models predict host species origin with high accuracy across the dataset. Interestingly, the age of host clade divergence positively associates with the degree of intraspecific microbial community distinguishability within the host clades, spanning recent host speciation (~one million years ago) to more distantly related host genera (~108 million years ago). Second, various topological congruence analyses of each group's phylogeny and microbiota dendrogram reveal significant degrees of phylosymbiosis, irrespective of host clade age or taxonomy. Third, experimental transplants of autochthonous (intraspecific) versus allochthonous (interspecific) microbiota among closely related wasp species and more divergent mice species demonstrate reductions in host survival and digestive performance, respectively. Consistent with selection on host-microbiota interactions driving phylosymbiosis, there are survival and performance reductions when interspecific microbiota transplants are conducted between closely-related and divergent host species pairs. Overall these findings indicate that the composition and functional effects of an animal's microbial community can be closely allied with host evolution, even across wide-ranging timescales and in diverse animal systems reared under controlled conditions.