The cotton aphid (Aphis gossypii Glover) is a cosmopolitan pest species consisting of various host plant-associated lineages that appear to have different patterns of insecticide resistance, electrophoretic banding, and reproductive output across alternative host species. Debate continues as to whether these differences represent intraspecific variation or indicate a complex of cryptic or sibling species. We studied the host plant-related ecology of two asexual lineages of A. gossypii associated with the families Malvaceae and Cucurbitaceae, respectively, in particular the host plant finding and acceptance processes of the alate forms. The two lineages proved to be differentiated across host plants in terms of: (1) their landing and settling behaviour, nymphal production rate, and subsequent colony establishment (i.e. nymphal survival and development) and (2) their sensory abilities in relation to host plant-derived odours. Furthermore, genetic structuring according to host plant type was detected using the gene for elongation factor 1-alpha. The magnitude of the genetic differentiation across lineages was low, perhaps indicating a relatively recent divergence. The results demonstrate: (1) the presence of (at least) two cryptic species within the current definition of A. gossypii, as anticipated in previous studies, and (2) the practicalities of using a multidisciplinary approach to understanding the limits of asexual species. If sexuals can be generated from each of these lineages, this conclusion will be open to further testing.