Serotonin is a ubiquitous neuromodulator that confers flexibility in networks to modulate a wide array of behavioral and physiological processes. However, due to the complexity and heterogeneity of serotonergic systems, it has been challenging to determine the patterns of connectivity as well as the physiological contexts that influence individual serotonin neurons. In this dissertation, I use two serotonergic neurons which innervate the Drosophila olfactory system, the CSDns, as a model to explore these broad questions comprehensively using anatomical approaches. I first show that the CSDns have distinct connectivity relationships with populations of antennal lobe principal olfactory neurons and that their output across is non-uniform across glomeruli. I then comprehensively explore the wiring logic of a CSDn at a single-cell level. I demonstrate that the CSDn is highly interconnected with local networks, receiving glomerulus-specific input and synapsing extensively with subtypes of local interneurons, but also receives top-down input from neurons extrinsic to the olfactory system. I further demonstrate that a single serotonin neuron can differ in its connectivity across sensory regions, even to the same neuron that spans both regions, suggesting that its interactions may also differ across regions. Lastly, I demonstrate that the CSDns affect olfactory behavior in a circadian manner and provide anatomical data suggesting that the CSDn receives input from a population of clock neurons. Taken together, this thesis reveals the complex connectivity of individually identifiable serotonergic neurons within and across sensory brain regions and explores potential sources of input across multiple scales (local, global, and temporal) which may regulate the CSDn in context-specific manners