Flow-induced K⁺ secretion in the aldosterone sensitive distal nephron is mediated by high conductance Ca²⁺-activated K⁺ (BK) channels. Familial hyperkalemic hypertension (pseudohypoaldosteronism type 2) is an inherited form of hypertension with decreased K⁺ secretion and increased Na⁺ reabsorption. This disorder is linked to mutations in genes encoding with-no-lysine kinase 1 (WNK1), WNK4, and Kelch-like 3/Cullin 3, two components of an E3 ubiquitin ligase complex that degrades WNKs. We examined whether the full length (or "long") form of WNK1 (L-WNK1) affected the expression of BK α subunits in HEK cells. Overexpression of L-WNK1 promoted a significant increase in BK α subunit whole-cell abundance and functional channel expression. BK α subunit abundance also increased with co-expression of a kinase dead L-WNK1 mutant (K233M) and with kidney specific WNK-1 (KS-WNK1), suggesting that the catalytic activity of L-WNK1 was not required to increase BK expression. A high K⁺ diet increases BK expression in intercalated cells. We examined whether dietary K⁺ intake affected L-WNK1 expression in the ASDN. We found a paucity of L-WNK1 labeling in cortical collecting ducts (CCDs) from rabbits on a low K⁺ diet, but observed robust staining for L-WNK1 primarily in intercalated cells when rabbits were fed a high K⁺ diet. Our results and previous findings suggest that L-WNK1 exerts different effects on renal K⁺ secretory channels, inhibiting ROMK and activating BK channels. A high K⁺ diet induced an increase in L-WNK1 expression selectively in intercalated cells and may contribute to enhanced BK channel expression and K⁺ secretion in CCDs.