Understanding complex population dynamics is critical for both basic and applied ecology. Analysis of genetic data has been promoted as a way to reconstruct recent non-equilibrium processes that influence the apportioning of genetic diversity among populations of organisms. In a structured-deme context, where individual populations exist as geographically distinct units, island biogeography theory and metapopulation genetics predict that the demographic processes of extinction, colonization, and migration will affect the magnitude and rate of genetic divergence between demes. New methods have been developed to attempt to detect the influence of non-equilibrium dynamics in structured populations. I challenged two of these methods: decomposed pairwise regression and allele frequency analyses, using simulations of genetic data from structured demes. I found that these methods suffer from a high type II error rate, or failure to reject the null hypothesis of mutation-migration-drift equilibrium for demes experiencing historical demographic events. In addition, island biogeography and metapopulation ecology predict that at equilibrium, some species in a patch will be recent colonists, as equilibrium indicates a balance between colonization of the patch and extinction from the patch. Recent colonists are unlikely to have reached population mutation-migration-drift equilibrium; hence a paradox exists between population and community level equilibrium. I used nuclear and mitochondrial genetic data from populations of two species of reptiles from the Turks and Caicos Islands, British West Indies to test for patterns of equilibrium vs. non-equilibrium. I found unexpected shallow genetic divergence in the Turks Island boa (Epicrates chrysogaster), indicating that this species likely existed as a panmictic population prior to the inundation of the Turks and Caicos Banks during the last glaciation. As the initial methods I tested using simulations proved unreliable, I used methods from phylogeography, landscape genetics, and island biogeography to detect significant non-equilibrium dynamics in the Turks and Caicos curly-tailed lizard (Leiocephalus psammodromus), finding evidence for high levels of biased gene flow. I propose that studies of genetic diversity on island archipelagos use tools from all three of these methods to evaluate empirical data in the context of equilibrium and the null hypotheses offered by island biogeography and population genetics theory. I frame the results both in the context of conservation and an understanding of equilibrium and non-equilibrium dynamics.