Adequate regulation of innate behaviours is crucial for survival. The ventral tegmental area (VTA) forms the core of the neural circuitry driving these motivated behaviours. VTA dopamine (VTA-DA) neurons encode reward and reward-predicting cues heterogeneously. Moreover, individual neurons respond to different behavioural and kinematic variables. However, it remains unclear whether individual dopamine neurons respond to competing rewards like feeding and voluntary exercise heterogeneously. Additionally, it is unknown how motivational state changes, such as hunger or enhanced exercise drive, influence these responses. The aim of this study was therefore to uncover how individual VTA-DA neurons encode competing rewards, and how motivational state affects their function.We performed 1-photon calcium imaging in DAT-cre mice expressing GCaMP6m in the VTA, while they freely explored an arena with multiple rewards, including food, water and a running wheel. To study the effects of increased drive for feeding and voluntary exercise, calcium activity of single neurons was recorded during food restriction and after repeated running wheel exposure. To assess the contribution of anatomically different subpopulations on food intake and locomotion, we optogenetically activated projection-specific VTA-DA neurons.We found that VTA-DA neurons encode food and voluntary exercise in an opposite manner, but not food and water. Similarly, projections to different targets controlled feeding and locomotion in an opposite manner. During food restriction and enhanced exercise drive, the responses of VTA-DA neurons became tuned to the prioritized reward. These results suggest that VTA-DA neuron subpopulations distinguish between competing rewards and shift their responses according to motivational state changes.