Polarized vesicular trafficking directs specific receptors and ion channels to the primary cilium, but the underlying mechanisms are poorly understood. Here we identify a key role for discs large MAGUK scaffold protein 1 (DLG1), a core component of the Scribble polarity complex, in regulating ciliary protein trafficking in kidney epithelial cells. Conditional knockout of Dlg1 in mouse kidney caused ciliary elongation and cystogenesis, and cell-based proximity labelling proteomics and fluorescence microscopy showed alterations in the ciliary proteome upon loss of DLG1. Specifically, serologically defined colon cancer antigen-3 (SDCCAG3) and intraflagellar transport protein 20 (IFT20), previously implicated in ciliary targeting of polycystin-2 (PC2), as well as PC2 itself, were reduced in cilia of DLG1 deficient cells compared to control cells. This phenotype was recapitulated in vivo and rescuable by re-expression of wildtype DLG1, but not a Congenital Anomalies of the Kidney and Urinary Tract (CAKUT)-associated DLG1 missense variant. Moreover, using biochemical approaches and Alpha Fold modelling we provide evidence that DLG1 associates physically with SDCCAG3 and IFT20, which in turn bind directly to each other. Our work thus identifies a key role for DLG1 in mediating ciliary targeting of PC2 and other proteins and implicates ciliary dysfunction as a possible contributing factor to CAKUT.