Chimeric antigen receptor (CAR) T cell therapy, while highly efficacious for the treatment of certain haematological malignancies, remains ineffective in solid cancers. Recent advances in CRISPR/Cas9 gene editing for primary T lymphocytes have presented new avenues for the precise engineering of armoured CAR T cells. We aimed to engineer CAR T cells to express cytokines under the transcriptional control of tumour-specific promoters, and hypothesised that this would enhance the safety and efficacy of armoured CAR T cells. This was achieved using a novel CRISPR/Cas9-mediated homology directed repair (CRISPR HDR) strategy to knock in (KI) proinflammatory cytokines into these gene loci expressed by T cells exclusively when within the tumour. This enabled the simultaneous deletion of inhibitory genes while achieving tumour-specific control of cytokine expression. Importantly this led to antigen-specific induction of transgene expression and improved cytotoxicity in tumour cocultures. In vivo, edited T cells exhibited tumour-specific transgene expression and improved anti-tumour efficacy in the OT-I transgenic TCR model. CRISPR HDR editing thus enables the generation of armoured CAR T cells with tumour-restricted cytokine secretion.