The population dynamics, development of gonads, takeoff and flight behaviour of Aphis gossypii Glover were investigated in order to test whether there was variation of migratory ability in the spring population. Field surveys showed that not all the aphids overwintering on hibiscus migrated to the secondary host plants, and the host-alternating and host-specific life-cycle forms coexisted in Nanjing, China. Substantial variation in flight capacity of winged individuals, development of gonads and takeoff behaviour were found within the spring population. The frequency distribution of flight duration and the number of ovarioles per individual alatae exhibited two peaks, representing the migratory and sedentary genotypes, respectively. Significant response to directional selection on takeoff behaviour demonstrated the additive genetic component of this variation. Selection for ‘takeoff’ individuals caused a significant increase in takeoff angle from 39.8° in the first selection to 68.7° in the fifth; and, hence, screened out the migratory genotype (M), while selection for the sedentary individuals increased the rate of non-takeoffs significantly, and screened out the sedentary genotype (S). The reciprocal cross, M♀×S♂, produced hybrid offspring performing significantly steeper takeoff angles compared with those from the cross S♀×M♂, suggesting the presence of a maternal effect. On the other hand, takeoff rate was ranked as M♀×S♂=S♀×M♂>M>S, involving no sex-linkage and maternal effect. The coexistence of host-alternating and host-specific life-cycle forms of A. gossypii on the primary host has, as deduced from the present studies, a genetic basis.