Conspicuous warning colours that signal chemical or other defences are common in the natural world. For instance, such aposematic warning patterns of red-and-black or yellow-and-black are common among insect taxa, particularly in the order Hemiptera, often forming the basis of Batesian and/or Müllerian mimicry rings. In addition, it has been repeatedly noted that colour polymorphisms or mutants that influence pigmentation can show pleiotropy with other behavioural, physiological or life-history traits. Here we describe a pale mutant of the seed bug Lygaeus simulans that appeared in our lab population in 2012, which differs in colour to the wild-type bugs. Through multigenerational experimental crosses between wild-type and pale mutant L. simulans, we first show that the pale phenotype segregates as a single Mendelian locus, with the pale allele being recessive to the wild-type. Next, we show (1) that there is a large heterozygous advantage in terms of fecundity, (2) that pale females suffer reduced longevity, and (3) that pale males have increased body length compared to wild-type homozygotes. Our data therefore suggest that the colour locus is pleiotropic with a number of life-history traits, opening the door for a more complete genetic analysis of aposematic colouration in this species. In addition, this phenotype will be useful as a visible genetic marker, providing a tool for investigating sperm competition and other post-copulatory drivers of sexual selection in this species.