Background:Insect-associated microorganisms can provide a wide range of benefits to their host, but insectdependency on these microbes varies greatly. The origin and functionality of insect microbiomes is not wellunderstood. Many caterpillars can harbor symbionts in their gut that impact host metabolism, nutrient uptake andpathogen protection. Despite our lack of knowledge on the ecological factors driving microbiome assemblages ofwild caterpillars, they seem to be highly variable and influenced by diet and environment. Several recent studieshave shown that shoot-feeding caterpillars acquire part of their microbiome from the soil. Here, we examinemicrobiomes of a monophagous caterpillar (Tyria jacobaeae) collected from their natural host plant (Jacobaeavulgaris) growing in three different environments: coastal dunes, natural inland grasslands and riverine grasslands,and compare the bacterial communities of the wild caterpillars to those of soil samples collected from underneatheach of the host plants from which the caterpillars were collected.Results:The microbiomes of the caterpillars were dominated by Proteobacteria, Actinobacteria, Firmicutes andBacteroidetes. Only 5% of the total bacterial diversity represented 86.2% of the total caterpillar’s microbiome.Interestingly, we found a high consistency of dominant bacteria within the family Burkholderiaceae in all caterpillarsamples across the three habitats. There was one amplicon sequence variant belonging to the genusRalstoniathatrepresented on average 53% of total community composition across all caterpillars. On average, one quarter of thecaterpillar microbiome was shared with the soil.Conclusions:We found that the monophagous caterpillars collected from fields located more than 100 km apartwere all dominated by a singleRalstonia. The remainder of the bacterial communities that were present resembledthe local microbial communities in the soil in which the host plant was growing. Our findings provide an exampleof a caterpillar that has just a few key associated bacteria, but that also contains a community of low abundantbacteria characteristic of soil communities.