Animals are host to a community of microbes, collectively referred to as their microbiome, that can play a key role in their hosts' biology. The bacterial endosymbionts of insects have a particularly strong influence on their hosts, but despite their importance we still know little about the factors that influence the composition of insect microbial communities. Here, we ask: what is the relative importance of host relatedness and host ecology in structuring symbiont communities of diverse aphid species? We used next-generation sequencing to compare the microbiomes of 46 aphid species with known host plant affiliations. We find that relatedness between aphid species is the key factor explaining the microbiome composition, with more closely related aphid species housing more similar bacterial communities. Endosymbionts dominate the microbial communities, and we find a novel bacterium in the genus Sphingopyxis that is associated with numerous aphid species feeding exclusively on trees. The influence of ecology was less pronounced than that of host relatedness. Our results suggest that co-adaptation between insect species and their facultative symbionts is a more important determinant of symbiont species presence in aphids than shared ecology of hosts.