In human-altered landscapes, species with specific habitat requirements tend to persist as metapopulations, forming colonies restricted to patches of suitable habitats, displaying mutually independent within-patch dynamics and interconnected by inter-colony movements of individuals. Despite intuitive appeal and both empirical and analytical evidence, metapopulations of only relatively few butterfly systems had been both monitored for multiple years to quantify metapopulation dynamics, and assayed from the point of view of population genetics. We used allozyme analysis to study the genetic make-up of a metapopulation of a declining and EU-protected butterfly, Euphydryas aurinia, inhabiting humid grasslands in western Czech Republic, and reanalysed previously published demography and dispersal data to interpret the patterns. For 497 colony x year visits to the 97 colonies known at that time, we found annual extinction and colonisation probabilities roughly equal to 4%. The genetic diversity within colonies was intermediate or high for all assessed parameters of population genetic diversity and hence higher than expected for such a habitat specialist species. All the standard genetic diversity measures were positively correlated to adult counts and colony areas, but the correlations were weak and rarely significant, probably due to the rapid within-colony population dynamics. Only very weak correlations applied to larval nests numbers. We conclude that the entirety of colonies forms a well-connected system for their majority. Especially in its core parts, we assume a metapopulation structure with a dynamic equilibrium between local extinction and recolonization. It is vital to conserve in particular these structures of large and interconnected colonies.Implications for insect conservation: Conservation measures should focus on considering more in depth the habitat requirements of E. aurinia for management plans and on stabilisation strategies for colonies, especially of peripheral ones, e.g. by habitat restoration.