Females that mate with multiple males (polyandry) may reduce the risk that their eggs are fertilized by a single unsuitable male. About 25 years ago it was hypothesized that bet-hedging could function as a mechanism favoring the evolution of polyandry, but this idea is controversial because theory indicates that bet-hedging via polyandry can compensate the costs of mating only in small populations. Nevertheless, populations are often spatially structured, and even in the absence of spatial structure, mate choice opportunity can be limited to a few potential partners. We examined the effectiveness of bet-hedging in such situations with simulations carried out under two scenarios; (1) intrinsic male quality, with offspring survival determined by male phenotype (male’s ability to generate viable offspring), and (2) genetic incompatibility (offspring fitness determined non-additively by parental genotypes). We find higher fixation probabilities for a polyandrous strategy compared to a monandrous strategy if complete reproductive failure due to male effects or parental incompatibility is pervasive in the population. Our results also indicate that bet-hedging polyandry can delay the extinction of small demes. Our results underscore the potential for bet-hedging to provide benefits to polyandrous females and have valuable implications for conservation biology.