Neuronal activity requires a vast amount of energy. Energy use in the brain is spatially and temporally dynamic, which reflects the changing activity of the neuronal circuits and might be important for modulating neuronal output. Much recent work has focused on understanding how brain glial cells take up nutrients from circulation and subsequently provide metabolic precursors to neurons. However, within the neurons, modulation of cellular metabolic pathway flux also regulates excitability and signaling. A coherent understanding of the links between energy availability and metabolism, neural signaling, and higher-level phenotypes like behavior requires a synthesis of the understanding of glial and neuronal metabolic dynamics. In the current review, we address this synthesis in the context of insect brain metabolism. Insects not only show evidence of a metabolic division of labor and plasticity in neural metabolism that closely resembles that observed in vertebrate species, there also seem to be direct links between brain metabolic dynamics and behavioral phenotypes. We summarize the current knowledge about the metabolic fuels available to the insect nervous system and how they are transported and distributed to the different neural cell types. We discuss the possibility of an ANLS-like metabolic division of labor between glial cells and neurons, and how it is regulated. We then discuss plasticity in flux through energy metabolic pathways in neurons, how flux is regulated, and how it influences neural signaling. We end by discussing how metabolic dynamics in the glia and neurons may interact to impact signaling.