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New species form when they become reproductively isolated. A classic model of speciation posits that derived mutations appear in isolated populations and reduce fitness when combined in hybrids. While these Bateson–Dobzhansky–Muller incompatibilities are known to accumulate as populations diverge over time, they may also reflect the amount of standing genetic variation within populations. We analysed the fitness of F 2 hybrids in crosses between 24 populations of a plant species ( Campanula americana ) with broad variation in standing genetic variation and genetic differentiation driven by post-glacial range expansions. Hybrid breakdown varied substantially and was strongest between populations near the historical cores of the species range where within-population genetic diversity was high. Nearly half of the variation in hybrid breakdown was predicted by the combined effects of standing genetic variation within populations, their pairwise genetic differentiation and differences in the climates they inhabit. Hybrid breakdown was enhanced between populations inhabiting distinct climates, likely reflecting local adaptation. Results support that the mutations causing hybrid breakdown, the raw material for speciation, are more common in long-inhabited areas of the species range. Genetic diversity harboured in refugial areas is thus an important source of incompatibilities critical to the speciation process.