Heritable microbial symbionts, vertically transmitted from maternal host to offspring, have made an indelible contribution to the ecology and evolution of life on earth. For instance, the fixation of symbionts in hosts contributed to pivotal biological shifts, such as the evolution of vascular plants and eukaryotic cells. Vertically transmitted symbionts are often specialized to host genotypes and confer fitness benefits to hosts, including protection against abiotic and biotic stress. Despite their ubiquity and strong influence on hosts, our understanding of what drives the prevalence and persistence of heritable symbionts lags behind that of macro-organisms. Two factors are theorized to determine equilibrium frequencies of heritable symbionts: 1) symbiont vertical transmission rates, and 2) the relative fitness of symbiotic and non-symbiotic hosts. Therefore, characterizing when and how these factors vary in host populations are necessary first steps to predicting the population dynamics of heritable symbionts. Here, I used large-scale field surveys, greenhouse and common garden experiments, as well as demographic modeling approaches to test the hypothesis that outcrossing (i.e., gene flow) between genetically distant hosts disrupts symbiosis. Specifically, host outcrossing is hypothesized to create genetic incompatibilities between sexually reproducing hosts and their specialized clonal symbionts, which may reduce both vertical transmission rates and symbiont mediated mutualistic benefits. First, I found that symbiont prevalence in one host species negatively associated with drought, while symbiont genotype explained residual variation in vertical transmission rates. These results suggest that symbiont genotype, and to a lesser extent, climate variables play roles in shaping symbiont population dynamics, but substantial variability was unexplained. Second, I manipulated gene flow between hosts along a gradient of genetic distances and determined that symbiont vertical transmission was robust to host outcrossing, which remained high for several host generations. Lastly, I quantified the net effect of host outcrossing on symbiont population dynamics. Contrary to our hypothesis, host outcrossing did not disrupt mutualistic benefits of symbiosis, and instead, buffered hosts against deleterious effects of outbreeding depression. Together, my work provides strong evidence that host outcrossing does not disrupt symbiosis, and alternatively demonstrates that heritable symbionts are important players in the population dynamics of outcrossing hosts.