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The genetic architecture of local adaptation has been of central interest to evolutionary biologists since the modern synthesis. In addition to classic theory on the effect size of adaptive mutations by Fisher, Kimura and Orr, recent theory addresses the genetic architecture of local adaptation in the face of ongoing gene flow. This theory predicts that with substantial gene flow between populations local adaptation should proceed primarily through mutations of large effect or tightly linked clusters of smaller effect loci. In this study, we investigate the genetic architecture of divergence in flowering time, mating system‐related traits, and leaf shape betweenMimulus laciniatusand a sympatric population of its close relativeM. guttatus. These three traits are probably involved inM. laciniatus’adaptation to a dry, exposed granite outcrop environment. Flowering time and mating system differences are also reproductive isolating barriers making them ‘magic traits’. Phenotypic hybrids in this population provide evidence of recent gene flow. Using next‐generation sequencing, we generate denseSNPmarkers across the genome and map quantitative trait loci (QTLs) involved in flowering time, flower size and leaf shape. We find that interspecific divergence in all three traits is due to fewQTLof large effect including a highly pleiotropicQTLon chromosome 8. ThisQTLregion contains the pleiotropic candidate gene TCP4 and is involved in ecologically important phenotypes in otherMimulusspecies. Our results are consistent with theory, indicating that local adaptation and reproductive isolation with gene flow should be due to few loci with large and pleiotropic effects.