1. The hoverfly Microdon myrmicae is a rare and extremely localised social parasite of Myrmica ants, only occurring around wet grassland. Dispersal, location of the host, and oviposition are crucial steps in the life of ant parasites but are poorly known due to the challenge of studying such rare species.2. Using genome-wide loci obtained by RADseq, we investigated the genetic structure and relatedness of Mi. myrmicae larvae and its ant host, collected from three localities in South West England, and inferred biological and behavioural traits.3. We found that: (a) Mi. myrmicae larvae show high inbreeding levels and severe heterozygosity deficiency, as an expression of the small population size that favours the mating between siblings or half-siblings; (b) Mi. myrmicae adults can disperse for many kilometres, spreading much more than it is reported for its sibling species, Microdon mutabilis; (c) a single female lays small egg bunches in different ant colonies, sometimes spanning substantial distances (bet-hedging strategy); in parallel, a single ant nest can harbour eggs from different Microdon females; (d) preliminary evidence suggest that contrary to Mi. mutabilis, host colony choice seems not to depend on the number of queens residing in a single colony.4. These results overall strongly deviate from what previously found for Mi. mutabilis, whose females oviposit in the natal nest generation after generation. We argue that such different ecological traits and parasitic strategies between closely related species are mainly ascribable to the different selective pressure on the two ant hosts.