Neuropeptide Y (NPY) in the arcuate nucleus (ARC) is known as one of the most critical regulators of feeding. However, how NPY’s promotion of feeding varies under different energy balance conditions is unclear. Therefore, we set out to determine the specific functional contributions of different ARC NPY neuronal population to different aspects of feeding behaviour and energy homeostasis control, and to investigate the underlying mechanistic drivers through which altered levels of NPY can promote feeding. For this, we utilised various transgenic mouse models and comprehensive phenotyping paradigms employing INTRSECT combined with chemogenetic DREADD and optogenetic manipulations as well as TRAP-RNAseq analysis to decipher their specific roles. These studies revealed that NPY derived from Agrp-positive neurons predominantly controls feeding and energy homeostasis under baseline conditions by signalling via lower-affinity post-synaptic NPY1R/NPY5R. However, under conditions of prolonged energy excess, as occurs in obesity, feeding is mostly driven by NPY originating from Agrp-negative NPY neurons preferentially signalling via the high affinity NPY2R located on POMC neurons. This suggests that under energy surplus conditions, when ARC NPY levels generally drop, high affinity NPY2R on POMC neurons are still able to drive food intake and enhance obesity development via NPY released predominantly from Agrp-negative NPY neurons.