A fundamental source of conflict in viviparous organisms stems from differences between maternal and paternal interests in resource allocation to offspring (i.e. parental conflict). Under parental conflict, variance in paternity drives the evolution of paternally derived, resource-acquiring alleles, and maternally derived alleles that distribute resources equally among offspring. In hybrids, mismatches between these parent-of-origin effect alleles can cause inappropriate development of essential nutritive tissues (e.g. placenta or endosperm), and subsequently embryo death. Here, I test the role of parental conflict in generating one of the most common intrinsic barriers in seed plants- Hybrid Seed Inviability (HSI)-using members of the evolutionary and ecological model system; the Mimulus guttatus species complex. I show that HSI has evolved rapidly and repeatedly in this group, and patterns of HSI conform to the predictions of parental conflict. Additionally, genetic mapping suggests that HSI is conferred by nuclear, parent-of-origin effect loci (i.e. loci that affect the probability of death only if maternally or paternally derived). Lastly, using a series of natural surveys and mixed pollination crosses, I find that species with different histories of parental conflict frequently co-occur and hybridize, and hybridization between species with differing histories of parental conflict can indirectly influence growth in non-hybrid seeds. Overall, this work highlights a dual role of parental conflict in the speciation process; both in the origin of reproductive isolation, but also in the dynamics and outcomes of hybridization in nature.