The navel orangeworm Amyelois transitella is an economically important pest of almonds and pistachios in California. Successful management at the correct spatial scale requires an understanding of insect dispersal, particularly relative to when mating occurs. A previous study found that unmated navel orangeworms were capable of flying longer distances than previously assumed, but it was not clear how mating affects dispersal in this species, nor how dispersal affects fecundity. To address these critical unknowns, females were allowed to fly on a flight mill on the night either before or after mating, and flight performance was assessed. Following the flight test, the females were set up for oviposition. The eggs produced were collected daily and monitored for fertility and compared to those produced by females that were minimally-handled and by tethered but unflown controls. Timing of flight relative to mating did not affect fecundity, nor did the distance or duration of flight. However, mated females flew significantly longer and farther than unmated moths. In addition, trials were conducted where females were forced to fly for predetermined periods of time up to 2 h. There was no effect of forced flight on fecundity. There was an increase in weight lost with time flown, but the effect was weak. The data from this study revealed no obvious trade-off between flight activity and reproductive output in female navel orangeworm. The results indicate that most females mate in or near their natal habitat, and some may disperse relatively long distances to oviposit elsewhere. It is also possible that the long flights by mated females observed on the flight mills represent appetitive ranging behavior, perhaps searching for oviposition host cues, rather than purposeful dispersal. In that case, net displacement in the field would be less because of meandering flight patterns. Although it is unclear if the navel orangeworm is a true migrant, mating is associated with different female behavior on the flight mills, including propensity to make longer-distance flights than unmated females. Long-flight capacity without loss of fecundity is an important feature contributing to the colonizing ability of this opportunistic pest.