Bacterial strains evolve in response to the gut environment of their hosts, with genomic changes that influence their interactions with hosts as well as with other members of the gut community. Great apes in captivity have acquired strains of Bacteroides xylanisolvens, which are common within gut microbiome of humans but not typically found other apes, thereby enabling characterization of strain evolution following colonization. Here, we isolate, sequence and reconstruct the history of gene gain and loss events in numerous captive-ape-associated strains since their divergence from their closest human-associated strains. We show that multiple captive-ape-associated B. xylanisolvens lineages have independently acquired gene complexes that encode functions related to host mucin metabolism. Our results support the finding of high genome fluidity in Bacteroides, in that several strains, in moving from humans to captive apes, have rapidly gained large genomic regions that augment metabolic properties not previously present in their relatives.