Small-cell lung cancer (SCLC) remains a fast-growing, genomically plastic neuroendocrine cancer with poor survival despite chemo-immunotherapy. Converging biological and clinical evidence identifies delta-like ligand 3 (DLL3) as a lineage-linked target expressed in most SCLC with limited normal tissue expression, enabling selective T-cell-based strategies. This review synthesises the trajectory of DLL3-directed therapies, positioning chimeric antigen receptor (CAR) T cells within a broader T-cell engagement continuum that now includes a clinically validated DLL3 × CD3 engager. We integrate preclinical and early clinical data to articulate a design blueprint for DLL3-directed CAR T cell in solid tumours: binder affinity tuned for on-target specificity; second- and third-generation signalling to balance rapid cytolysis with persistence; and armouring modules, such as IL-7/ CCL19 or IL-18, to counter hypoxia, poor trafficking and immune suppression in the SCLC tumour microenvironment. Using a representative next-generation DLL3-directed CAR T-cell platform as an example, we highlight the translational importance of shortened manufacturing that preserves T-cell stemness and may facilitate dose optimisation and improve treatment feasibility. We also set out a biomarker framework that links antigen density, longitudinal DLL3 assessment in tissue and liquid biopsies and pharmacodynamic tracking of expansion and persistence to patient selection and retreatment. Finally, we outline a pragmatic trial agenda that prioritises step-up dosing, built-in control features and rational combinations with radiotherapy or checkpoint blockade to mitigate toxicity and reduce antigen escape. Together, these engineering, biomarker and clinical design principles provide a framework for evaluating DLL3-directed CAR T-cell therapies in future clinical studies.