Recent studies show that intraspecific genetic variation in asexual species may have large effects on community and ecosystem functions, increasing their stability, productivity, and species richness. However, major questions regarding its population-level impact remain empirically unanswered: (a) How does intraspecific genetic diversity affect the ecological characteristics of sexual species, in which recombination can alter the outcome of causal mechanisms such as selection and niche diversification? (b) Does genetic diversity increase population dynamic stability? (c) Is the impact of genetic diversity dependent on the selective environment? To answer these questions, I founded replicate flour beetle (Tribolium castaneum) populations with different degrees of ecologically relevant, heritable trait variation and monitored their dynamics for approximately eight generations. I show that population stability and persistence increased with greater genetic variation but that the stabilizing effect was independent of the selective habitat (different proportions of ancestral and novel resources). Alleles from a single founding strain underwent a selective sweep in the homogeneous ancestral habitat but not in a novel heterogeneous habitat. These results expand current understanding of the ecological impacts of genetic diversity by showing that genetically more diverse sexual populations persist longer and are more stable but that the selective environment determines the mechanistic basis of increased stability.