Host shifts are considered a key generator of insect biodiversity. For insects, adaptation to new host plants often requires changes in larval/pupal development and adult behavioural preference toward new hosts. Neurochemicals play key roles in both development and behaviour and therefore provide a potential source for such synchronization. Here, we correlated life-history timing, brain development and corresponding levels of 14 neurochemicals in (Diptera: Tephritidae), a species undergoing ecological speciation through an ongoing host shift from hawthorn to apple fruit. These races exhibit differences in pupal diapause timing as well as adult behavioural preference with respect to their hosts. This difference in behavioural preference is coupled with differences in neurophysiological response to host volatiles. We found that apple race pupae exhibited adult brain morphogenesis three weeks faster after an identical simulated winter than the hawthorn race, which correlated with significantly lower titres of several neurochemicals. In some cases, particularly biogenic amines, differences in titres were reflected in the mature adult stage, when host preference is exhibited. In summary, life-history timing, neurochemical titre and brain development can be coupled in this speciating system, providing new hypotheses for the origins of new species through host shifts.