Adaptive behavior requires both innate and learned behaviours, but little is known about the interactions of the circuitry underlying these behaviours, or the implications of this on the evolution of behaviour. Using the olfactory response to trimethylamine (TMA) in the Mus clade as a cross-species model, we explored changes in the circuitry of innate behaviour through plasticity and evolution. TMA is a volatile odour produced during putrefaction and is aversive to most mammals. However, Mus musculus evolved to produce TMA as a social signal and are attracted to it. We demonstrate a concentration-dependent response of Mus musculus to TMA, while Mus caroli show an aversive response. In addition, Mus musculus' innate response to TMA can be modified by learning, and requires TMA exposure in order for attraction to develop. To investigate the neurobiological substrate of this behaviour, we performed activity-dependent labelling of cells in the Anterior Olfactory Nucleus (AON) and cortical amygdala (CoA) to express excitatory opsins or inhibitory DREADDs. Our findings demonstrate that cells active during TMA olfaction are necessary and sufficient for attraction in Mus musculus, while the CoA is neither necessary nor sufficient. Furthermore, we use light sheet microscopy to analyse whole-brain c-Fos and Arc expression in Mus musculus and Mus caroli following TMA exposure. By directly comparing the brains of two closely related species with contrasting behavioural responses to a single stimulus, our study sheds light on how evolution and plasticity together shape neuronal circuitry to drive adaptive changes in behaviour.