The western terminus of State Route 264 is located at its junction with US 160 in Moenkopi, adjacent to Tuba City.

The highway curves back towards the south until it reaches the northern terminus of SR 87 in Second Mesa.

SR 264 continues east to a junction with US 191 in Burnside and the two run concurrently until they reach Ganado.

SR 264 continues east to Window Rock, where the highway reaches its eastern terminus at the New Mexico state line.

The route from Tuba City to Window Rock existed as a dirt road as early as 1927.

[5] By 1956, a large gap in the road was completed through Hah-Hoh-No-Geh Canyon, just southeast of Tuba City.

[6] In previous years, this gap had made the driving the road between Hotevilla and Tuba City impossible.