Many neurons receive synapses in stereotypic proportions from converging but functionally distinct afferents. However, developmental mechanisms regulating synaptic convergence are not well understood. Here we describe a heterotypic mechanism by which one afferent controls synaptogenesis of another afferent, but not vice versa. Like other CNS circuits, zebrafish retinal H3 horizontal cells (HC) undergo an initial period of remodelling, establishing synapses with ultraviolet and blue cones while eliminating red and green cone contacts. As development progresses, the HCs selectively synapse with ultraviolet cones to generate a 5:1 ultraviolet-to-blue cone synapse ratio. Blue cone synaptogenesis increases in mutants lacking ultraviolet cones, and when transmitter release or visual stimulation of ultraviolet cones is perturbed. Connectivity is unaltered when blue cone transmission is suppressed. Moreover, there is no cell-autonomous regulation of cone synaptogenesis by neurotransmission. Thus, biased connectivity in this circuit is established by an unusual activity-dependent, unidirectional control of synaptogenesis exerted by the dominant input.