The lifetime dispersal of an individual determines the gene flow and invasion potential of the species. Linking dispersal to population growth remains a challenging task and is a major knowledge gap, for example, for conservation management. We utilized 20 year mark-recapture data on two extensive nest-box populations of Siberian flying squirrels in western Finland to analyze lifetime dispersal patterns and to study relative roles of different demographic rates behind population growth. Natal dispersal means the distance between the natal nest and the nest used the following year, whereas breeding movements refers to the nest site changes between breeding attempts. The movement distances we observed were comparable to distances reported earlier from radio telemetry studies. We observed that breeding movements did not contribute to lifetime dispersal distance. In other words, juveniles were responsible for redistributing individuals within and between populations. Based on an integrated population model, which estimated all relevant annual demographic rates (birth, local apparent survival, and immigration) as well as population growth rates, immigration was the demographic rate which showed clear correlations to annual population growth rates in both populations. That is, flying squirrels may persist in a network of uncoupled subpopulations, where dispersal between subpopulations is of critical importance. Our study supports the view that dispersal has the key role in population survival of a small forest rodent and natal dispersal is the process determining consequences of movement ecology of the species at the population level.