Reproductive proteins tend to diverge unusually rapidly between species. This pattern is frequently attributed to post-mating sexual selection. However, despite many well-characterized examples of rapidly evolving reproductive proteins, little data exist which directly address this widely invoked hypothesis. The Heliconius genus of butterflies offers a good opportunity to examine this hypothesis by contrasting patterns of reproductive protein evolution between clades with divergent mating systems: adult-mating and pupal-mating. With few exceptions, pupal-mating females mate only once, which severely limits the opportunity for post-mating sexual selection to act. In contrast, adult-mating females mate repeatedly throughout life, providing ample opportunity for post-mating sexual selection to drive the adaptive evolution of reproductive proteins. Thus theory predicts that reproductive protein evolution should be slower in the pupal-mating clade relative to the adult-mating clade. Focusing initially on two species, H. erato (pupal-mating) and H. melpomene (adult-mating), I used a combination of expression, bioinformatic, and proteomic to identify 51 putative seminal fluid proteins. Evolutionary rate estimates based on pairwise alignments reveal these Heliconius seminal fluid proteins evolve more rapidly than a set of ~300 'non-reproductive' proteins derived from wing tissue. To further explore evolutionary patterns of reproductive proteins in Heliconius and to compare mating systems, I sequenced 20 seminal fluid protein genes from 10 more Heliconius species and an outgroup. Applying codon-site models to these data indicated three proteins with dN/dS greater than 1, strongly implicating positive selection in the rapid evolution of at least a few Heliconius seminal fluid proteins. Comparison evolutionary rates between clades yielded the result that, contrary to predictions, the average evolutionary rate of seminal fluid proteins is greater among pupal-mating Heliconius. These results suggest that positive selection and relaxed constraint can generate conflicting signals when examining patterns of reproductive protein evolution across mating systems. As predicted, some loci may show elevated evolutionary rates in promiscuous taxa relative to monandrous taxa resulting from adaptations to postmating sexual selection. However, when monandry is derived (as in Heliconius), the opposite pattern may result from relaxed constraint of loci formerly influenced by post-mating sexual selection.