The ecological plasticity of aphid populations is determined by their clonal and morphotypic diversity. Clones will be successful when the development of their component morphotypes is optimized. The purpose of this work was to reveal the peculiarities of clonal composition and the developmental characteristics of different summer morphotypes for the rose-grass aphid, Metopolophium dirhodum (Walk.), which is an important host-alternating cereal pest and a useful model species. During the experiments, aphids were kept under ambient conditions on wheat seedlings at natural temperatures and humidity levels. An analysis of the reproduction of summer morphotypes and the resulting composition of offspring found that variation among the clones and morphotypes, as well as generational effects and an influence of sexual reproduction (and interactions between all factors) influenced the population structure of M. dirhodum. The reproduction of emigrants was less among the clones than that of the apterous or alate exules. The number of offspring produced by apterous exules differed throughout the growing season (generational effects) and between years, with different clones exhibiting different responses. There were dispersing aphids only among the offspring of apterous exules. These results can contribute to future advances in the forecasting and monitoring of aphid populations.