In autoimmune disorders, CD4 T cell-dependent chronic B cell activation towards multiple self-antigens promotes the production of pathogenic autoantibodies. However, the molecular signature and precise phenotype of autoreactive CD4 T cells in human autoimmunity have been elusive, even more so for rare diseases like autoimmune hepatitis (AIH). Here, we combined brief ex vivo restimulation with pools of overlapping antigen-derived peptides and integrative single-cell RNAseq (scRNAseq) to characterize the circulating CD4 T cell response against Soluble Liver Antigen (SLA or SepSecs) in seropositive (defined as positive for anti-SLA auto-antibodies) and seronegative AIH patients. Only seropositive AIH patients had detectable amounts of SLA-specific CD4 T cells, which had a conserved memory CXCR5neg PD-1high CCR6neg phenotype, and an atypical B helper molecular profile with high expression of IL21, IFNG, TIGIT and CTLA4 among other genes. Strikingly, the expanded SLA-specific CD4 TCR clonotypes identified by scRNAseq were only found in the circulating CXCR5neg PD-1high CD4 T cell population, which was significantly increased in the blood of AIH patients and shared B helper capacity with the classical CXCR5high PD-1high CD4 TFH population. Altogether, our results provide for the first time a fine and comprehensive characterization of autoreactive CD4 T cells in the rare autoimmune disorder AIH, thereby identifying the phenotypic niche and specific molecular signature of pathogenic B helper self-reactive CD4 T cells.