In many songbirds, vocal learning-related cellular plasticity was thought to end following a developmental critical period. However, mounting evidence in one such species, the zebra finch, suggests that forms of plasticity common during song learning continue well into adulthood, including a reliance on auditory feedback for song maintenance. This reliance wanes with increasing age, in tandem with age-related increases in fine motor control. We investigated age-related morphological changes in the adult zebra finch song system by focusing on two cortical projection neuron types that a) share a common efferent target, b) are known to exhibit morphological and functional change during song learning, and c) exert opposing influences on song acoustic structure. Neurons in HVC (proper name) and the lateral magnocellular nucleus of the anterior nidopallium (LMAN) both project to the robust nucleus of the arcopallium (RA). During juvenile song learning and adult song maintenance, HVC promotes song syllable stereotypy while LMAN promotes learning and acoustic variability. Following retrograde labeling of these two cell types in adults, there were age-related increases in dendritic arbor in HVC-RA but not LMAN-RA neurons, resulting in an increase in the ratio of HVC-RA:LMAN-RA dendritic arbor. Differential growth of HVC relative to LMAN dendrites may relate to increases in song motor refinement, decreases in the reliance of song on auditory feedback, or both. Despite this differential growth with age, we also show that both cell types retain the capacity for experience-dependent growth. These results may provide insights on mechanisms that promote and constrain adult vocal plasticity.