In many animals, food intake is strictly regulated by sensory, homeostatic, and hedonic neural circuits that balance energy intake with energy expenditure. Although neural circuits that regulate food intake have been extensively investigated in rodent models, the entire sensory-motor neural circuits that generate food perception and accordingly regulate food ingestion have not been fully understood in any model organism. We use the fly (Drosophila melanogaster) to understand the fundamental principles of how the brain integrates the sensory percept of food with the sensation of hunger and satiety to regulate food intake on the level of circuits. Previously, we identified a novel group of interneurons, IN1 neurons, as a regulator of food ingestion in flies. Here, we used optogenetics and two-photon calcium imaging to investigate the neural circuitry of IN1 neurons. We found that IN1 neurons receive specific excitatory input from sugar-sensing chemosensory neurons and mechanosensitive neurons that respond to food texture. Using, intersectional genetics, we investigated which sugar-sensing neurons activate IN1 neurons. Our detailed analysis showed that taste neurons expressing Gr43a generated a strong and sustained calcium response in IN1 neurons. We further investigated which Gr43a neurons produce this excitatory effect and found that IN1 neurons receive specific excitatory input from interoceptive Gr43a neurons that innervate the fly digestive system. Finally, we developed a new imaging preparation to capture the activity of gut neurons in vivo in behaving flies. Using this imaging prep, we showed that Gr43a gut neurons indeed respond to sugar ingestion. Our research revealed that the gut-brain axis might regulate food ingestion in flies in a similar way to in rodents and humans.