The zebra finch (Taeniopygia guttata) songbird learns a “tutor” song during a single developmental critical period (CP), offering a window through which to study the neural mechanisms that enable the learning of complex behaviors. Zebra finch song relies on interactions among distributed multimodal brain regions, and maintaining a balance between hemispheric specialization and interhemispheric coordination may be essential. Accordingly, the zebra finch may also be a suitable model organism in which to study comparative mechanisms of interhemispheric integration. In this dissertation, I describe the use of longitudinal resting-state fMRI (rs-fMRI) functional connectivity (FC) analyses to offer insights into these topics. In Chapter 1, I detail the extensive methodological innovations that were required to develop our novel zebra finch rs-fMRI pipeline. These included the creation of (1) a custom zebra finch brain template; (2) the NeuroViz toolbox, used to digitally extract the zebra finch brain and delineate regions of interest; and (3) the MRIqual toolbox, used for rs-fMRI quality assurance. In Chapter 2, I show that the zebra finch brain exhibits brain-wide bilaterally symmetric intrinsic brain activity (i.e., homotopic FC), consistent with interhemispheric coordination for complex behaviors. Homotopic FC is identified across Eutherian (placental) mammals, and the corpus callosum (CC), unique to this clade, is thought to structurally mediate this functional architecture. Chapter 2 provides the first indication that homotopic FC extends further across vertebrate phylogeny, suggesting that the CC is not a requirement for homotopic FC in normal ontogeny. In Chapter 3, I use the methodological and analytic techniques developed in previous chapters to identify FC signatures of tutor experience during the CP for song learning. It is known that tutor experience regulates neural plasticity within the caudomedial nidopallium (NCM), a higher-order auditory region integral for tutor song memorization. Chapter 3 extends these findings by showing that tutor experience also influences the centrality of left NCM within large-scale functional brain networks. Collectively, these chapters constitute the first reports of whole-brain rs-fMRI analyses in the zebra finch. The methodological advances and empirical findings presented here could help to pave the way for future investigations using rs-fMRI to answer comparative neuroscience questions.