<p>Limb regeneration in insects can impose physiological costs that create trade-offs with reproduction, but whether these costs are modulated by mate choice and extend to population-level consequences remains unclear. Using the ladybird beetle, <i>Cheilomenes sexmaculata</i>, we investigated how leg regeneration interacts with mate choice (female choice, male choice, and no-choice settings) to influence mating behaviour, reproductive output, offspring development, and population growth. Our results reveal that neither females nor males discriminate against regenerated partners, indicating that limb regeneration is not used as a mate assessment cue. However, significant hidden costs emerged post-copulation that were strongly dependent on both regeneration status and choice context. Control females that chose regenerated males suffered severe reductions in fecundity and fitness, while control males that chose regenerated females produced offspring with significantly extended development, a novel transgenerational cost. Crucially, no-choice control pairs outperformed choice treatments across multiple parameters, demonstrating that mate choice itself can be costly when assessment cues are unreliable. At the population level, regenerated individuals, particularly in choice-based matings, reduced the intrinsic rate of increase and extended doubling time, suppressing population growth. These findings reveal that regeneration carries context-dependent costs that are often amplified, rather than mitigated, by mate choice. This creates a potential evolutionary trap where individuals cannot behaviourally avoid costly matings, with implications for life-history evolution, sexual selection theory, and biological control programs.</p>