Insular fauna face disproportionate risks of extinction owing to direct human perturbation and intrinsic factors that are enhanced at small population sizes. Currently, our understanding of the processes that promote long-term persistence of naturally small populations and the cryptic processes that may contribute to accelerating their decline is limited by lack of empirical investigations across the range of natural conditions. Implementing effective protections for rare and understudied taxa requires the identification and examination of factors that limit recruitment at critical life stages. Predicting population health outcomes of future perturbations further necessitates an understanding a taxon’s behavioral ecology. Finally, cryptic threats to viability, such as inbreeding depression, must be investigated with an appreciation for taxon-specific life history, as these attributes can alter the context in which severe fitness reductions are expressed. In this project I enlist integrative and cross-disciplinary approaches to study the behavioral ecology and conservation genetics of a critically endangered West Indian Rock Iguana, Cyclura nubila caymanensis, on Little Cayman Island. I demonstrate how coastal communal nesting areas, a critical limiting resource on the island, serve a diverse population demographic and contribute to significantly enhanced nesting outcomes. These data emphasize the importance of expanding protections for major sites, as aggregative nesting appears to be perpetuated by both habitat suitability and adaptive fitness benefits. I next evaluate the possibility of evolved inbreeding avoidance strategies, including natal dispersal, non-assortative mate choice, and genetic bet-hedging. I conclude that the contribution of pre-reproductive dispersal to inbreeding avoidance likely outweighs that of active mate choice. Importantly, observed patterns of siring success imply constrained female choice and sexual conflict over genetic mating outcomes – a pattern that may extend to many territorial, male-driven mating systems and therefore should be an important consideration in genetic management. Finally, I investigate age-dependent inbreeding effects and the degree to which inbreeding depression may limit recruitment to the breeding population. I fail to reveal significant correlations of multi-locus heterozygosity with hatchling fitness; however, negative effects of parental inbreeding on fecundity and hatching success imply fitness consequences of inbreeding depression could be felt at other life stages.