Neuropeptide Y (NPY) in the arcuate nucleus (ARC) is known as one of the most critical regulators of feeding. However, how NPY promotes feeding under obese conditions is not known. Here we show that at least two functionally distinct NPY neuronal population exist in the ARC, defined by the presence or absence of Agrp. Paradoxically, ablation of NPY only from Agrp neurons produces a mild obesity phenotype in mice characterised by increased food intake and an upregulation of Npy2r. Importantly, we also show that positive energy balance induced by HFD in general, or in genetically obese leptin receptor-deficient mice, leads to elevated Npy2r expression especially on POMC neurons. Utilising INTRSECT technology to specifically only activate the newly discovered circuitry of Agrp-negative NPY neurons via DREADD’s leads to strongly increased feeding specifically via these POMC Npy2r’s, while optogenetic inhibition of the Agrp-negative NPY neurons reduces feeding. Consistent with that, lack of Npy2r on POMC neurons leads to reduced food intake and fat mass under positive energy balance conditions. Together, this indicates that under normal energy balance conditions, NPY derived from Agrp-positive neurons predominantly acts on lower affinity Npy1r to control feeding. While under energy surplus conditions, when NPY levels drop, signalling via the high affinity Npy2r on POMC neurons is still able to drive food intake and enhance obesity development via NPY released from Agrp-negative NPY neurons.