Microbial communities are a key component of host health. As the microbiota is initially ‘foreign’ to a host, the host's immune system should respond to its acquisition. Such variation in the response should relate not only to host genetic background, but also to differences in the beneficial properties of the microbiota. However, little is known about such interactions. Here, we investigate the gut microbiota of the bumblebee, Bombus terrestris, which has a protective function against the bee's natural trypanosome gut parasite, Crithidia bombi. We transplanted ‘resistant’ and ‘susceptible’ microbiota into ‘resistant’ and ‘susceptible’ host backgrounds, and studied the activity of the host immune system. We found that bees from different resistance backgrounds receiving a microbiota differed in aspects of their immune response. At the same time, the elicited immune response also depended on the received microbiota's resistance phenotype. Furthermore, the microbial community composition differed between microbiota resistance phenotypes (resistant versus susceptible). Our results underline the complex feedback between the host's ability to potentially exert selection on the establishment of a microbial community and the influence of the microbial community on the host immune response in turn.