Lehtimäki et al. reveal how repulsive Slit1b/2-Robo2 and attractive neurturin-Gfrα1/2-Ret signaling jointly coordinate multipolar migration of horizontal cells through crowded, scaffold-free environments of the vertebrate retina. This work was enabled by sophisticated transcriptomics analysis, targeted F0 CRISPR screening, and 3D fixed and live imaging.