Characterizing how frequently, and at what life stages and spatial scales, dispersal occurs can be difficult, especially for species with cryptic juvenile periods and long reproductive life spans. Using a combination of mark–recapture information, microsatellite genetic data, and demographic simulations, we characterize natal and breeding dispersal patterns in the long-lived, slow-maturing, and endangered Blanding’s turtle (Emydoidea blandingii), focusing on nesting females. We captured and genotyped 310 individual Blanding’s turtles (including 220 nesting females) in a central Wisconsin population from 2010 to 2013, with additional information on movements among 3 focal nesting areas within this population available from carapace-marking conducted from 2001 to 2009. Mark–recapture analyses indicated that dispersal among the 3 focal nesting areas was infrequent (<0.03 annual probability). Dyads of females with inferred first-order relationships were more likely to be found within the same nesting area than split between areas, and the proportion of related dyads declined with increasing distance among nesting areas. The observed distribution of related dyads for nesting females was consistent with a probability of natal dispersal at first breeding between nearby nesting areas of approximately 0.1 based on demographic simulations. Our simulation-based estimates of infrequent female dispersal were corroborated by significant spatial genetic autocorrelation among nesting females at scales of <500 m. Nevertheless, a lack of spatial genetic autocorrelation among non-nesting turtles (males and females) suggested extensive local connectivity, possibly mediated by male movements or long-distance movements made by females between terrestrial nesting areas and aquatic habitats. We show here that coupling genetic and demographic information with simulations of individual-based population models can be an effective approach for untangling the contributions of natal and breeding dispersal to spatial ecology.