Horizontal cells are inhibitory interneurons with dendritic fields that overlap one another, contacting the pedicles of cone photoreceptors. Because of their regular spacing, they provide a uniform coverage of the retinal surface. The developmental mechanisms establishing their morphological properties are undefined, but cell-intrinsic instructions and interactions with neighboring cells have each been suggested to play a role. Using a variety of inbred and genetically-modified strains of mice, we have modulated the relationship between horizontal and cone cell numbers to study the role of homotypic and afferent density upon horizontal cell differentiation. Variation in horizontal cell density produces a corresponding change in the size of the dendritic field, while altering cone density leaves dendritic field size unaffected but drives higher order dendritic branching and terminal clustering. Functional dendritic overlap is achieved anatomically at the level of individual pedicles, where horizontal cells interact as they colonize pedicles based upon their relative proximity. Afferent and homotypic interactions therefore generate the network properties of horizontal cells that underlie their functional coverage.