Each fall, eastern North American monarch butterflies (Danaus plexippus) use a time-compensated sun compass to migrate to their overwintering grounds in central Mexico. The sun compass mechanism involves the neural integration of skylight cues with timing information from circadian clocks to maintain a constant heading. The neuronal substrates for the necessary interactions between compass neurons in the central complex, a prominent structure of the central brain, and circadian clocks are largely unknown. To begin to unravel these neural substrates, we performed 3D reconstructions of all neuropils of the monarch brain based on anti-synapsin labeling. Our work characterizes 21 well-defined neuropils (19 paired, 2 unpaired), as well as all synaptic regions between the more classically defined neuropils. We also studied the internal organization of all major neuropils on brain sections, using immunocytochemical stainings against synapsin, serotonin, and γ-aminobutyric acid. Special emphasis was placed on describing the neuroarchitecture of sun-compass-related brain regions and outlining their homologies to other migratory species. In addition to finding many general anatomical similarities to other insects, interspecies comparison also revealed several features that appear unique to the monarch brain. These distinctive features were especially apparent in the visual system and the mushroom body. Overall, we provide a comprehensive analysis of the brain anatomy of the monarch butterfly that will ultimately aid our understanding of the neuronal processes governing animal migration.