Glucocorticoid (GC) hormones have well characterised roles for the development of several fetal organs, however, specific developmental roles of GCs in the fetal kidney are relatively unknown. We have explored both the expression and localisation of the glucocorticoid receptor (GR) within developing kidney structures during organogenesis and the effect of eliminating GR expression using gene-targeted GR-null mice. We show that loss of the GR has a profound effect on the renal transcriptome with altered expression of 454 genes in the GR-null mouse kidney at E18.5 of gestation with more genes significantly downregulated (305) than upregulated (99) relative to wild-type controls, including the key primary cilia-associated gene Centrosomal protein 290 (Cep290) with a fold change of -3.6. Two renal tubule markers, Kidney androgen regulated protein (Kap) (proximal tubule marker) and S100 calcium binding protein G (S100g) (distal tubule marker) were also downregulated with fold changes of -8.61 and -2.5 respectively. We demonstrate that primary cilium length is significantly decreased in kidney proximal tubule cells in E18.5 GR-null mice (5.23 + 0.12, µm + SEM) compared with wild type controls (6.27+ 0.15, µm + SEM). Finally, we demonstrate that in the IMCD3 mouse collecting duct cell line dexamethasone treatment increases the length of primary cilia compared to vehicle controls (vehicle 2.49 + 0.03, µm + SEM vs dexamethasone 3.17 + 0.05 µm + SEM), an effect blocked by pre-treatment with the GR antagonist RU486. Taken together these results indicate that GC signalling via the GR contributes to the formation of primary cilia in the proximal tubule and is required for normal kidney development.