Changes in dendritic morphology in response to activity have long been thought to be a critical component of how neural circuits develop to properly encode sensory information. Ventral-preferring direction-selective ganglion cells (vDSGCs) have asymmetric dendrites oriented along their preferred direction, and this has been hypothesized to play a critical role in their tuning. Here we report the surprising result that visual experience is critical for the alignment of vDSGC dendrites to their preferred direction. Interestingly, vDSGCs in dark-reared mice lose their inhibition-independent dendritic contribution to direction-selective tuning while maintaining asymmetric inhibitory input. These data indicate that different mechanisms of a cell's computational abilities can be constructed over development through divergent mechanisms.