Crohn’s disease is a chronic, multifactorial inflammatory disease impacting the gastrointestinal system, with a significant genetic component to disease risk. Genetic association studies have advanced our biological understanding of Crohn’s disease and therapeutic development. However, the majority of Crohn’s disease genetic associations (>300 loci) reside in non-coding regions with unknown biological mechanisms, leaving them unleveraged. Additionally, current therapeutics for Crohn’s disease are not equally effective across patients, underscoring the need for a better understanding of disease biology and genetics-led drug discovery. We leveraged a large blood single-cell eQTL cohort (TenK10K Phase I, n = 1,925), and Crohn’s disease GWAS summary statistics (N = 59,957 (NFE), 367,586 (meta)) to identify genes with cell type-specific pleiotropic effects on Crohn’s disease and gene expression. We applied summary data-based multi-instrument Mendelian Randomisation developed for two independent eQTL and GWAS cohorts. We identified 510 genes (pSMR multi FDR<0.05) across 28 blood cell types, and correlated expression between immune cells from blood and gastrointestinal tissue to support the utility of single cell-blood eQTL. We developed a holistic prioritisation score for each gene based on biological plausibility, bulk eQTL MR results from relevant tissues, monogenic immune disease databases, and differential expression in Crohn’s disease. We found that the prioritised genes participate in gene regulatory networks that are dysregulated in a cell type-specific manner in Crohn’s disease tissue, highlighting the transcription factors IRF1 and ZBTB38 and their target genes in CD4+ and CD8+ T cells. We investigated the therapeutic potential of targeting these pathways by non-viral, exogenous delivery of mRNA in primary T cells from healthy individuals in vitro, paired with deep molecular and cellular profiling. Preliminary evidence supports ZBTB38, CCDC88B and SYNGR1 as T cell-specific therapeutic targets. In summary, our work contributes towards genetics-led development of RNA-based therapeutics to target cell type-specific pathway dysregulation in Crohn’s disease.