Significance Connections are crucial to brain function and a variety of molecular systems direct axonal growth during development and regeneration. An important system involves Celsr2, Celsr3, and Fzd3, membrane proteins that also regulate epithelial planar cell polarity (PCP). Here, we show genetically that Celsr2 and Celsr3 guide axons redundantly, in collaboration with Fzd3 in the same cell populations. However, unlike in epithelial PCP, their action is Vangl1 and Vangl2 independent. Furthermore, expression of Celsr2-3 and Fzd3 in thalamocortical axons and cortical cells is required for the fine mapping of cortical areas. Our findings that Celsr2, Celsr3, and Fzd3 regulate axonal guidance using mechanisms different than epithelial PCP have implications for brain wiring during normal development and regeneration.