We experimentally and theoretically investigated the persistence of hosts and parasitoids interacting in a metapopulation structure consisting of ephemeral local patches (MELPs). We used a host–parasitoid system consisting of necrophagous Diptera species and their pupal parasitoids. The basal resources used by the host species were assumed to be ephemeral, supporting only one generation of individuals before completely disappearing from the environment. We experimentally measured the host–parasitoid persistence and the effects of local demographic processes in two scenarios: 1) constant occurrence of basal resources at a single site (no dispersion or colonization of other sites) and 2) variable occurrence of basal resources between two sites (colonization of a new patch requiring species dispersal). The experimental setup and findings were then formalized into a mathematical model describing the interaction dynamics in a MELP structure. We evaluated the contribution of several factors to the host–parasitoid coexistence, such as resource allocation probability (probability of resource appearance in a site), variation in resource size and number of sites available to receive resources in the MELP. We found that demographic fluctuations and environmental stochasticity affected the density of migrants, patch habitat connectivity, persistence and spatial distribution of interacting species.