Sensory neuronopathies (SNN) and small fiber neuropathies (SFN) are debilitating disorders often associated with neuropathic pain, yet their underlying mechanisms remain poorly understood. Autoantibodies against fibroblast growth factor receptor 3 (α-FGFR3) have been identified in a subset of patients, but their pathological significance has not been established. Here, we describe that α-FGFR3-positive patients consistently report neuropathic pain and display a distinct clinical phenotype characterized by large-fiber involvement and non-length-dependent fiber loss, suggesting dorsal root ganglia (DRG) dysfunction. We demonstrate that α-FGFR3 bind to sensory neurons within dorsal root ganglia (DRG). We validated both at the transcript and protein level that the target of autoantibodies, FGFR3, is expressed in human sensory neurons and that therefore α-FGFR3 could find their target in primary afferents. DRG neurons exposed to α-FGFR3 rapidly acquired a hyperexcitability phenotype. Injection of α-FGFR3-positive patient serum in rats caused mechanical hypersensitivity, mirroring patient-reported pain symptoms. Mechanistically, α-FGFR3 activated the Mitogen-activated protein kinases (MAPK) signaling cascade, specifically extracellular signal-regulated kinase (ERK) and p38, which are known to enhance neuronal excitability. Epitope mapping revealed key extracellular epitopes on FGFR3. Blocking these epitopes prevented α-FGFR3-induced sensory neuron hyperexcitability, thus showing that the autoantibody binding of the FGFR3 extracellular domain is a key factor affecting DRG neurons. Our work suggests that beyond their role as biomarkers, α-FGFR3 actively contribute to pain hypersensitivity by acting on the DRG. This positions both α-FGFR3 and FGFR3 signaling as a potential therapeutic targets for modulating sensory neuron excitability and treating autoimmune neuropathies.