T helper 17 (Th17) cells play critical roles in inflammatory and autoimmune diseases. The lineage‐specific transcription factor RORγt is the key regulator for Th17 cell fate commitment. A substantial number of studies have established the importance of transforming growth factor β (TGF‐β) ‐dependent pathways in inducing RORγt expression and Th17 differentiation. TGF‐β superfamily members TGF‐β₁, TGF‐β₃ or activin A, in concert with interleukin‐6 or interleukin‐21, differentiate naive T cells into Th17 cells. Alternatively, Th17 differentiation can occur through TGF‐β‐independent pathways. However, the mechanism of how TGF‐β‐dependent and TGF‐β‐independent pathways control Th17 differentiation remains controversial. This review focuses on the perplexing role of TGF‐β in Th17 differentiation, depicts the requirement of TGF‐β for Th17 development, and underscores the multiple mechanisms underlying TGF‐β‐promoted Th17 generation, pathogenicity and plasticity. With new insights and comprehension from recent findings, this review specifically tackles the involvement of the canonical TGF‐β signalling components, SMAD2, SMAD3 and SMAD4, summarizes diverse SMAD‐independent mechanisms, and highlights the importance of TGF‐β signalling in balancing the reciprocal conversion of Th17 and regulatory T cells. Finally, this review includes discussions and perspectives and raises important mechanistic questions about the role of TGF‐β in Th17 generation and function.