1. We describe the pattern of colonization of suitable, but currently empty, habitat by a host butterfly and two specialist parasitoids living in a highly fragmented landscape. 2. Using survey data collected over 8 years, field sampling and small-scale experiments we show that the ability of the Glanville fritillary butterfly (Melitaea cinxia) to colonize new habitat is intermediate between that of its two larval primary parasitoids. 3. The butterfly forms a classic metapopulation, which the parasitoid Hyposoter horticola experiences as a single patchily distributed host population because of its high rate of dispersal and long colonization distances. In contrast, most of the local butterfly populations are presently inaccessible to the parasitoid Cotesia melitaearum, which has a limited dispersal range and therefore persists only in tightly clustered networks of host populations. 4. At the regional scale, the butterfly may escape C. melitaearum by colonizing empty habitat, but host dispersal does not limit parasitism by H. horticola, which consequently must be limited by local interaction. 5. The parasitoid H. horticola mostly avoids direct competition with C. melitaearum because the majority of H. horticola populations are outside the range of dispersal by current C. melitaearum populations. In contrast, all C. melitaearum populations experience competition with H. horticola. none