Diverse organisms actively manipulate their (sym)biotic and physical environment in ways that feedback on their own development. However, the degree to which these processes affect microevolution remains poorly understood. The gazelle dung beetle both physically modifies its ontogenetic environment and structures its biotic interactions through vertical symbiont transmission. By experimentally eliminating i) physical environmental modifications, and ii) the vertical inheritance of microbes, we assess how environment modifying behavior and microbiome transmission shape heritable variation. We found that depriving larvae from symbionts and environment modifying behaviors increased additive genetic variance and heritability for development time but not body size. This suggests that larvae’s ability to manipulate their environment has the potential to modify heritable variation and to facilitate the accumulation of cryptic genetic variation. This cryptic variation may become released and selectable when organisms encounter environments that alter the degree to which they can be manipulated. Furthermore, we found heritable variation for the response to the elimination of environmental modifications, indicating that genotypes differ in their dependence on the ability to manipulate their environment. Our findings highlight that the ability of organisms to actively manipulate their environment may affect the potential of populations to evolve when encountering novel, stressful conditions.