The primary olfactory centres of the sphinx moth Manduca sexta, the antennal lobes, contain a small number of sexually dimorphic glomeruli: the male-specific macroglomerular complex and the large female glomeruli. These glomeruli play important roles in sex-specific behaviours, such as the location of conspecific females and the selection of appropriate host plants for oviposition. The development of sexually dimorphic glomeruli depends strictly on the ingrowth of sex-specific olfactory receptor cell afferents. In the present study we tested the role of female-specific olfactory receptor cells (ORCs) in mediating female-specific host plant approach behaviour and in determining the response of downstream antennal lobe neurons. We generated male gynandromorphs by excising one imaginal disc from a male larva and replacing it with the antennal imaginal disc from a female donor. Most male gynandromorphs had an apparently normal female antenna and a feminised antennal lobe. These gynandromorphs were tested for flight responses in a wind tunnel towards tomato plants, a preferred host plant for oviposition in M. sexta. Male gynandromorphs landed on host plants as often as normal females, demonstrating that the presence of the induced female-specific glomeruli was necessary and sufficient to produce female-like, odour-oriented behaviour, i.e. orientation towards host plants. We also characterised the physiological and morphological properties of antennal lobe neurons of male gynandromorphs. We found that projection neurons with arborisations in the induced female-specific glomeruli showed physiological responses akin to those of female-specific projection neurons in normal females. These results therefore indicate that ORCs confer specific odour tuning to their glomerular targets and, furthermore, instruct odour-specific behaviour.