The S. cerevisiae guanine nucleotide exchange factor (GEF) Cdc24 regulates polarized growth by binding to Cdc42, a Rho-type GTPase that has many effectors, including Ste20 kinase that activates multiple MAPK cascades. Here, we show that Cdc24 promotes MAPK signaling during mating through interactions with Ste5, a scaffold that must shuttle through the nucleus and bind to the beta subunit (Ste4) of a G protein for Ste20 to activate the tethered MAPK cascade. Ste5 is basally recruited to growth sites of G1 phase cells independently of Ste4. Loss of Cdc24 inhibits nuclear import and blocks basal and pheromone-induced recruitment of Ste5. Ste5 is not basally recruited and MAPK Fus3 is not basally activated in the presence of a mutant Cdc24 (G168D) that still activates Cdc42, suggesting that Cdc24 regulates Ste5 and the associated MAPK cascade through a function that is not dependent on its GEF activity. Consistent with this, Cdc24 binds Ste5 and co-precipitates with Ste4 independently of Far1 and Ste5. Loss of Cdc24 decreases Ste4-Ste5 complex formation and loss of Ste4 stimulates Cdc24-Ste5 complex formation. Collectively, these findings suggest that Cdc24 mediates site-specific localization of Ste5 to a heterotrimeric G protein and may therefore ensure localized activation of the associated MAPK cascade.