Investigating relationships between microbiota and their host is essential toward a full understanding of how animal adapt to their environment. Lake Whitefish offers a powerful system to investigate processes of adaptive divergence where the dwarf, limnetic species evolved repeatedly from the normal, benthic species. We compared the transient intestinal microbiota between both species from the wild and in controlled conditions, including their reciprocal hybrids. We sequenced the 16s rRNA gene V3‐V4 regions to (a) test for parallelism in the transient intestinal microbiota among sympatric pairs, (b) test for transient intestinal microbiota differences among dwarf, normal, and hybrids reared under identical conditions, and (c) compare intestinal microbiota between wild and captive whitefish. A significant host effect on microbiota taxonomic composition was observed when all lakes were analyzed together and in three of the five species pairs. In captive whitefish, host effect was also significant. Microbiota of both reciprocal hybrids fell outside of that observed in the parental forms. Six genera formed a bacterial core which was present in captive and wild whitefish, suggesting a horizontal microbiota transmission. Altogether, our results complex interactions among the host, the microbiota, and the environment, and we propose that these interactions define three distinct evolutionary paths of the intestinal microbiota. Investigating the holobiont system is essential toward a full understanding of how animal adapt to their environment and, ultimately, speciation. We compared and sequenced the transient intestinal microbiota among dwarf and normal forms as well as their reciprocal hybrids of Lake Whitefish from the wild and in controlled conditions. Our results suggest complex interactions among the host, the microbiota, and the environment.