Plant viruses transmitted by aphids cause tremendous losses around the world. The primary mode of virus transmission is the noncirculative manner where viruses are retained on specific receptors located in aphid stylets. Viruses are transported on the stylet’s surface, while the aphid moves from plant to plant. They are inoculated often within a single puncture, thereby promoting viral outbreaks. In this context, the identification of receptors of viruses within their insect vectors is a key challenge to understanding the mechanisms of transmission, and offers an avenue for future alternative control strategies to limit viral spread. We developed several approaches to characterize and identify plant virus receptors in aphid stylets. These approaches include, amongst others, fine-tune dissection of insect mouthparts for in vitro interaction assays with viruses, immunolabeling with specific antibodies, high-resolution microscopies or proteomics analyses and RNAi silencing and targeted mutagenesis in aphids to validate gene candidate receptors. All this work as first been developed using the Cauliflower mosaic virus as model, and should benefit to other vector-transmitted noncirculative viruses. We discovered the acrostyle at the tip of aphid maxillary stylets (1), organ that displays plant virus receptors all over its surface (2). We determined the first proteome of insect stylets and identified the proteins present at the surface of the acrostyle, named stylins. And more importantly, we mapped peptides at the interface of virus-vector interactions. Our results allowed the identification of the first receptor of noncirculative plant viruses, the protein Stylin-01 shown to play a key role in Cauliflower mosaic virus transmission (3), and provide novel insights into virus-vector interactions. They also revealed that the acrostyle is a multifaceted organ with various binding properties and functions.