Abstract Sexual selection, and conflicts between sex or within sex, can induce morphological variations within species. This may challenge the identification and characterization of diagnostic morphological characters from reproductive organs that are of utmost importance for the morphology-based classification of faunal diversity, particularly on species level. In Lepidoptera, and in some other insects, females have evolved reproductive organs that can accommodate and/or digest nuptial gifts, or so called spermatophores, transferred from the males during copulation. The properties of the spermatophores principally depend on the male’s condition, which is defined by resources acquired and depleted across life stages. In these conditions, the size and/or shape of the female reproductive organs are likely to differ visually between females of different mating status, and with their mates’ condition. The widespread African monarch, Danaus chrysippus, can host an endosymbiotic bacterium, Spiroplasma that induces son-killing in this species. When prevalent, such symbionts distort their host population sex-ratio, which can increase the reproduction load on the few uninfected males, lead to a local excess of unmated females, and resource-depletion in males. Here, we characterized variation in the female genitalia across populations with different levels of Spiroplasma infection. First, virgin females have smaller organs, while mated females show expanded organs; and further, females from highly female-biased and male-killing Spiroplasma infected populations have a larger area of their corpus bursae covered with signa structures. These observations potentially suggest that females from populations that are male depleted may have evolved an efficient mechanical way to optimize the digestion of small nutritious spermatophores.