Repetitive stereotyped behaviors are core symptoms of autism spectrum disorders (ASD) and fragile X syndrome (FXS), the prevalent genetic cause of intellectual disability and autism. The nigrostriatal dopamine (DA) circuit is key to movement control and creation of habits and sequential behaviors, thus its dysregulation could promote occurrence of autistic repetitive behaviors. However, specific evidence proving altered nigral DA neuron activity in ASD or FXS models is absent. In this study, by analyzing nigral DA neuron activity in adolescent Fmr1 KO mice by ex vivo electrophysiology we provide direct evidence of early dysregulation of the nigrostriatal DA circuit in the FXS model. Moreover, by performing immunofluorescence, Western blot experiments, and intracerebral drug injections coupled to ex vivo electrophysiology or behavioral tasks, we reveal the molecular substrates of nigral DA neuron dysregulation and repetitive behaviors, that involve the interplay between metabotropic glutamate receptor 1 (mGluR1) and ErbB tyrosine kinases, receptors for the neurotrophic and differentiation factors known as neuregulins. Lastly, we show that systemic ErbB inhibition concurrently corrects nigral DA neuron dysfunctions and repetitive behaviors in the FXS model. In conclusion, our evidence demonstrates that nigral DA neuron hyperactivity is an early signature of FXS, nigral mGluR1 and ErbB play a role in FXS pathology, and targeting ErbB is a valuable pharmacological approach to treat core symptoms of ASD and FXS.