Cactoblastis cactorum (Berg) (Lepidoptera: Pyralidae) is an invasive herbivore that poses a serious risk to Opuntia cacti in North America. Knowledge of the flight behavior of the cactus moth is crucial for a better understanding of natural dispersal, and for both monitoring and control. We used computer-linked flight mills to investigate diel flight activity and flight performance in relation to gender, age, mating status, and body size. Maximal flight activity for both mated and unmated moths occurred during twilight, whereas flight activity was low during photophase. The total distance flown and the number of initiated flights within a diel cycle were higher in both unmated and mated females than in males, but the longest single flight was similar in both genders. These findings suggest that pheromone trap captures of males likely indicate the simultaneous presence of females and that mated females might even be in areas where males are not detected yet. Flight performance heterogeneity was large, with a small portion of the population (both males and females) performing long unbroken flights, whereas the majority made short flights. Females had higher pupal and adult body size and shorter longevity than males. A few individuals, particularly young mated females, flying long distances may be important for active spread of a population and the colonization of new habitats. Implications of this study in the control of the cactus moth by using the sterile insect technique are discussed.