Angioimmunoblastic T-cell lymphoma (AITL) is a neoplastic proliferation of T follicular helper cells with clinical and histological presentations suggesting a role of antigenic drive in its development. Genetically, it is characterized by a step-wise acquisition of somatic mutations, with early mutations involving epigenetic regulators (TET2, DNMT3A) and occurring in haematopoietic stem cells, while subsequent changes involving signaling molecules (RHOA, VAV1, PLCG1, CD28) critical for T-cell biology. To search for evidence of potential oncogenic cooperation between genetic changes and intrinsic TCR signaling, we investigated somatic mutations and T-cell receptor β (TRB) rearrangement in 119 AITL, 11 peripheral T-cell lymphomas with T follicular helper phenotype (PTCL-TFH) and 25 PTCL-NOS by Fluidigm PCR and Illumina MiSeq sequencing. We confirmed frequent TET2, DNMT3A and RHOA mutations in AITL (72%, 34%, 61%) and PTCL-TFH (73%, 36%, 45%) and showed multiple TET2 mutations (2-3) in 57% of the involved AITL and PTCL-TFH. Clonal TRB rearrangement was seen in 73 cases with multiple functional rearrangements (2-4) in 18 cases (24%). On selected cases, we confirmed bi-clonal T-cell populations and further demonstrated that these independent T-cell populations harbored identical TET2 mutations by BaseScope in situ hybridization, suggesting their derivation from a common TET2 mutant progenitor cell population. Furthermore, both T-cell populations express CD4. Finally, in comparison with tonsillar TFH cells, both AITL and PTCL-TFH showed a significant over-representation of several TRB variable family members, particularly TRBV19*01. Our findings suggest the presence of parallel neoplastic evolutions from a common TET2 mutant haematopoietic progenitor pool in AITL and PTCL-TFH albeit to be confirmed in a large series of cases. The biased TRBV usage in these lymphomas suggests that antigenic stimulation may play an important role in predilection of T-cells to clonal expansion and malignant transformation.