Identifying patterns, and ascertaining causes, of the current distribution of genetic variation is often difficult in natural systems. Historical legacies and complex interactions among multiple abiotic and biotic processes lead to sometimes weak inference. One way to tackle this complexity is to study systems that allow for control or constraint of some variables. My thesis employs multiple natural experiments to carefully study the influence of dispersal and selection on population genetic structure through three focal studies. First, I use a meta-analysis of paired taxa (controlling for species age and environment) to identify correlates of gene flow. I found broad support for a positive relationship between dispersal potential and gene flow and in the exceptions find results that suggest the influence of genetic drift and natural selection. Second, I track the multi-year ecological and genetic recovery of three species from a die-off along the central coast of California to reveal how dispersal potential relates to rates of larval recruitment and spatial genetics. Species with higher dispersal potential re-colonized a broader extent of the impacted range, and did so more quickly, than species with lower dispersal potential, suggesting species’ attributes (e.g. fecundity, pelagic duration, and population size) can influenced realized dispersal. Third, I capture the genetic consequences of a high mortality (83% loss) marine epizootic in an intertidal keystone predator by comparing specimens collected the year before the outbreak with survivors after the outbreak, and comparing these each to newly recruited juveniles during the outbreak. Patterns in changing allele frequencies in candidate loci suggest natural selection is the main driver contributing to changes observed in this system, rather than genetic drift or gene flow. This series of natural experiments uses a framework aimed at predicting the influence of a suite of life-history traits — e.g. fecundity, pelagic duration, and population size — on population genetic differentiation, including how patterns of recruitment (spatial and genetic) are shaped by dispersal and its interaction with the filtering effects of natural selection.