In the wing dimorphic milkweed-oleander aphid, Aphis nerii, winged aphids begin reproducing about 1.5 days after wingless aphids. The longer maturation period is primarily due to slower development since even adult eclosion by winged aphids takes place after wingless aphids begin reproducing. The delay is not due to a post-eclosion, pre-reproductive flight since, beginning with the fourth instar, larval winged aphids were reared at a density of one per plant and the vast majority were not stimulated to fly under such low-density conditions. Thus, the ability to fly incurs a fitness cost in terms of delayed reproduction, irrespective of whether flight actually occurs. We did not observe a difference between morphs for lifetime fecundity, even though wingless aphids have larger abdomens than winged aphids and for both morphs there is a significant correlation between abdomen width and fecundity. Offspring produced by wingless aphids over the first four days of reproduction are larger than those produced by winged aphids, and the size difference at birth is maintained into adulthood. However, there are no differences in life history traits between these offspring, including maturation period and lifetime fecundity. Thus, reduced body size does not increase the cost of being able to fly, at least under the conditions of these experiments. The cost of being able to fly in this species should favor reduced production of winged individuals in populations that exploit more permanent host plants.