Steroids exert powerful effects on the brains and behavior of many species, but measures and manipulations of endocrine physiology in songbirds often reveal unexplained connections between steroids and the brain. The zebra finch song system, a sensorimotor neural circuit sensitive to steroids throughout life, organizes and functions largely in apparent independence from gonadally-derived steroids. We test the hypothesis that the zebra finch brain has the capacity for de novo steroidogenesis and that neurally-synthesized steroids, neurosteroids, may impact the song system. Using multiple techniques, we demonstrate that the steroidogenic acute regulatory protein (StAR), cytochrome P450 side chain cleavage (CYP11A1), and 3-hydroxysteroid dehydrogenase/5-4 isomerase (3-HSD), the first three factors in the steroidogenic pathway, are expressed in both developing and adult zebra finch brain. Detailed expression mapping at posthatch day 20 (P20) and adult reveals widespread area-specific expression and co-expression patterns for StAR, CYP11A1, and 3-HSD which suggest neurosteroids may modulate multiple brain functions, including sensory and motor systems. Notably, while expression of other steroidogenic genes such as aromatase has been essentially absent from the song system, each of the major song nuclei express at least a subset of steroidogenic genes described here, establishing the song system as a potential steroidogenic circuit.