Over the last two decades, the universe of insect taste has significantly expanded, from the initial identification of receptors expressed on peripheral neurons to the elucidation of complete neuronal circuits governing memory, locomotor output, homeostasis, and numerous behaviors associated with feeding. In parallel, neurobiologists have leveraged the genetic workhorse Drosophila melanogaster in both its larval and adult form to pursue these directions, with each developmental stage affording unique advantages as a model system for dissecting taste. Our work includes efforts to optimize the process of behavioral data analysis in adults, where we develop an adaptable pipeline for high-resolution analyses of multiple features associated with feeding on liquid food sources. Using this approach and established choice behavior assays, we identify the regulation of appetitive tastant feeding via pharyngeal gustatory receptor neuron (GRN) populations, and specifically a subset of pharyngeal GRNs that express sugar receptor Gr43a. However, how taste sensing and feeding behavior is shaped across metamorphosis is less understood. To better understand the taste system’s influence on behavior across development, we first developed a model for larval tastant exposure that permits us to assay adult behavior using non-toxic amounts of bitter tastants. We identified that exposure to certain tastants as larvae imbued attenuated avoidance to innately aversive tastants as adults across behavior assays such as food choice and proboscis extension responses. This shift in behavior was specifically linked to the identity of the tastant encountered during larval development. Additionally, we observed that behavioral modification required both functional bitter taste and intact mushroom body and dopaminergic neuron activity, where gustatory memory is formed and stored. Our results suggest that attenuation of avoidance to innately bitter compounds may require multiple levels of putative taste circuits, from the periphery to central processing components. Interestingly, silencing of dopaminergic neurons implicated in learned avoidance seemed to potentiate avoidance behavior, revealing the required regulation of learned aversion pathways in habituating avoidance. Overall, this work represents the first genetic and circuit-wide dissection of how a tastant response may be modulated across development following exposure during early life.