When possible, oviparous females should deposit eggs in sites that maximize the future performance of their offspring. Therefore, studies of oviposition behavior may uncover parameters important to offspring fitness. Gravid female Aedes albopictus (Skuse) were given a choice of containers with leaf infusion or plain water, either open or with a cover with a small opening, and their behavior was compared under summer (long day, higher temperature) or fall (short day, lower temperature) regimes. Open containers with leaf infusion were always preferred, but over time, summer females expanded their choices to oviposit in all containers and follow-up experiments indicated that the number of eggs laid was inversely correlated to the number of eggs present. In contrast, fall females laying diapausing eggs that do not hatch until the spring, accumulated eggs in open containers with food resulting in high egg densities. Combined, these results demonstrate a seasonal shift that suggests either high winter egg mortality or safety in numbers. It also demonstrates that female Ae. albopictus change their behavior based on cues associated with expected added risk, which varies across time and space. The wide distribution of summer eggs across container types may contribute to the fast expansion of Ae. albopictus across its invasive range, but egg accumulation in the fall may be exploited for control.