Neuronal cilia have emerged as pivotal signaling hubs; yet the ciliary molecules that organize signaling modalities and communication with neighboring synapses remain elusive. To map the brain cilia proteome, we engineered an Arl13b-TurboID mouse that enabled robust cilia-specific biotinylation in all cell types. Comparative quantitative proteomics revealed that neuronal and kidney cilia share less than half of their proteome. The brain cilia proteome encompasses synaptic proteins, transporters, adhesion molecules, and neurotransmitter receptors. Surprisingly, several signaling and adhesion molecules localize on neuronal cilia in discrete patterns, which are actively established. Mapping the NMDA receptor GluN1 at 25 nm resolution in the mouse cortex revealed a close, non-random association between ciliary GluN1 molecules and neighboring glutamatergic synapses. Cilia may thus eavesdrop on synaptic communication by re-deploying parts of the synaptic apparatus. Our study highlights the diversity and specialization of mammalian ciliary proteomes and indicates that nanoscopic organization may endow neuronal cilia with extrasynaptic functions.