Gene duplications can facilitate adaptation and may lead to inter-population divergence, causing reproductive isolation. We used whole-genome re-sequencing data from 34 butterflies to detect duplications in two Heliconius species, H. cydno and H. melpomene. Taking advantage of three distinctive signals of duplication in short-read sequencing data, we identified 744 duplicated loci in H. cydno and H. melpomene, 96% of which were validated with single molecule sequencing. We have found that duplications overlap genes significantly less than expected at random in H. melpomene, consistent with the action of background selection against duplicates in functional regions of the genome. Duplicate loci that are highly differentiated between H. melpomene and H. cydno map to four different chromosomes. Four duplications were identified with a strong signal of divergent selection, including an odorant binding protein and another in close proximity with a known wing colour pattern locus that differs between the two species.