Contextual cues are important triggers for overeating, but little is known about the neural mechanisms involved in acquiring this behaviour to begin with. We sought to understand the contribution of hunger-sensitive agouti-related peptide-expressing neurons (AgRP neurons) in acquiring context-induced feeding (CIF) behaviour in mice, using a model that requires mice to be fasted during the training phase. Given that AgRP neurons underpin a hunger-driven feeding response, we hypothesised they may also be critical for hunger-mediated acquisition of CIF which results in fed mice over-eating to a specific context. We first addressed whether AgRP neurons are required for fasting-driven CIF independent of an acute feeding response by chemogenetically inhibiting AgRP neurons in AgRP-Gi mice prior to 30 min training sessions in a discrete context (context A). When we tested all mice under fed conditions in the absence of treatment, we found that AgRP-Gi mice failed to discriminate their food intake in context A versus an alternate context (context B) (A vs B; p<0.05), suggesting AgRP neurons are necessary to acquire CIF in fasted mice independent of a historical feeding response. To assess sufficiency in fed mice, we employed two excitatory approaches, 1. chemogenetic activation of AgRP neurons with CNO prior to training (AgRP-Gq: n=6; AgRP-WT: n=7), and 2. optogenetic activation of AgRP neurons restricted to the training context (AgRP-ChR: n=5 ; AgRP-WT: n=10). Both approaches drove spontaneous feeding during training (Gq vs WT: p<0.05; ChR vs WT: p<0.05), however, only the optogenetic approach was sufficient for CIF expression at test (ChR p<0.05; Gq p=0.98), suggesting AgRP neurons facilitate CIF through dynamic changes in neuronal firing. Together we highlight an important functional dissociation between acute and conditioned feeding mediated by AgRP neurons, and suggest the timing of neuronal silencing is critical to achieve the latter.