Earthworms carry species-specific, Verminephrobacter symbionts in their nephridia (excretory organs) The symbionts are vertically transmitted via the cocoon, they can only colonize the host during early embryonic development, and have co-speciated with their host for about 100 million years. Although several studies have addressed the Verminephrobacter diversity between worm species, the intra-species diversity of the symbiont population has never been investigated. To address symbiont population structure, we used a multi-locus sequence typing (MLST) approach on Verminephrobacter isolated from two contrasting ecological types of earthworm hosts: the high population density, fast reproducing compost worms, Eisenia andrei and E. fetida, and the low-density, slow reproducing Aporrectodea tuberculata, commonly found in garden soils; for both types, three distinct populations were investigated. Based on MLST of 193 Verminephrobacter isolates, the symbiont community in each worm individual was very homogeneous. The more solitary A. tuberculata carried unique symbiont populations in 9 out of 10 host individuals, whereas the symbiont populations in the social compost worms were homogeneous across host individuals from the same population. Thus, host ecology shapes the population structure of the Verminephrobacter symbionts. The homogeneous symbiont populations in the compost worms indicate that Verminephrobacter can be transferred bi-parentally or via leaky horizontal transmission in high-density, frequently mating worm populations.