This research addresses the scaling of neural investment and behavioral complexity in the avian song system. Prior analyses demonstrated that the size of premotor song control regions (SCR) is related to the size of the song repertoire performed, suggesting that SCR size conveys functional capability. Here, detailed measures of singing behavior and its neuroanatomical basis in the Carolina wren Thryothorus ludovicianus are presented. This species was chosen for its potential to inform comparative studies relating brain and behavior at multiple levels of analysis; evaluations of brain:behavior scaling within this species (intra- and intersexual), as well as interspecific comparisons within the genus, are presented. Behavioral measures include estimates of repertoire sizes, as well as measures of song output and type-switching during singing. Objective methods for evaluating the syllabic structure of song are also presented. Neuroanatomical measures were based on nuclei HVc and RA in the song motor pathway, and include measures of neuron size and density. An immunohistochemical method for evaluating synapse density is also presented. The distinct syllable “types” of the Carolina wren song repertoire are shown to contain multiple, stable “forms”; this result requires reconsideration of the actual unit of learning and production (song “type” versus “form”). Song system synapse density estimates from males of two species having song repertoires of very different size were equivalent, suggesting that synapse density is not a marker of repertoire diversity. The relationship between neural investment in SCR and song repertoire size differs markedly among levels of analytical scale. Nearly all aspects of SCR cytoarchitecture differ between singing males and non-singing females, suggesting that neural investment is scaled inter-sexually to the performance of song. However, these same neuroanatomical measures fail to explain variation in singing behavior among individual males, suggesting that neural investment and singing behavior are uncoupled at this level. Nonetheless, overall SCR volume, as well as nucleus RA neuron size and density, are related to song repertoire size among species within this genus. This “taxon level effect” suggests that the factors relating brain and behavior in this genus do not act similarly within and among species