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Abstract The evolution of postzygotic isolation is thought to be a key step in maintaining species boundaries upon secondary contact, yet the dynamics and persistence of hybrid incompatibilities in naturally hybridizing species are not well understood. Here, we explore these issues using genetic mapping in three independent populations of recombinant inbred lines between naturally hybridizing monkeyflowers,Mimulus guttatusandMimulus nasutus,from the sympatric Catherine Creek population. We discover that the threeM. guttatusfounders differ dramatically in admixture history, with nearly a quarter of one founder's genome introgressed fromM. nasutus. Comparative genetic mapping in the three RIL populations reveals three new putative inversions, each one segregating among theM. guttatusfounders, two due to admixture. We find strong, genome‐wide transmission ratio distortion in all RILs, but patterns are highly variable among the three populations. At least some of this distortion appears to be explained by epistatic selection favouring parental genotypes, but tests of inter‐chromosomal linkage disequilibrium also reveal multiple candidate Dobzhansky‐Muller incompatibilities. We also map several genetic loci for hybrid pollen viability, including two interacting pairs that coincide with peaks of distortion. Remarkably, even with this limited sample of threeM. guttatuslines, we discover abundant segregating variation for hybrid incompatibilities withM. nasutus,suggesting this population harbours diverse contributors to postzygotic isolation. Moreover, even with substantial admixture, hybrid incompatibilities betweenMimulusspecies persist, suggesting postzygotic isolation might be a potent force in maintaining species barriers in this system.