Selective pressures throughout evolutionary history have caused the adaptation of sex-specific responses to dilemmas that are relevant for reproductive fitness. Sex differences in imagined jealousy due to infidelity are well documented, but past work does not consider the influence of reproductive capability (i.e., being fertile versus infertile) on responses. Relying on an online survey of 369 adults, we hypothesized that infidelities involving an infertile interloper lead to less jealousy than infidelities involving a fertile interloper. Further, for sexual infidelity, regardless of the interloper’s fertility, we hypothesized men would allocate the most responsibility to their partner and women would do so for the interloper, given women are assumed to behave with more intention. This hypothesis was partially supported; while men did allocate the most responsibility to their mate, so too did women, but women also blamed the interloper more than men. With regards to emotional infidelity, again independent of the interloper’s fertility, we hypothesized men will primarily hold their partner responsible. However, we hypothesized that when women will again consider the interloper responsible, but also their partner, due to concerns over fear of losing access to needed resources. This prediction was partially supported, as both sexes primarily hold their partner most responsible, and women held the interloper more accountable than did men. The findings shed light onto how individuals assess relationship threats and allocate responsibility, according to the reproductive capability.