In 741, as Japan staggered through the aftermath of a catastrophic smallpox epidemic that had swept the country between 735 and 737, Emperor Shomu issued an extraordinary edict. A Buddhist monastery and nunnery would be established in each of Japan's provinces, the kokubunji system, temples built from a semi-standardized template intended to promote Buddhism as the state religion and extend imperial authority to the most remote corners of the realm. The Hida Kokubun-ji rose in what is now central Takayama around 757, making it one of the later provincial temples to be completed. The temple belongs to the Koyasan Shingon-shu sect, and its honzon, the principal object of worship, is a statue of Yakushi Nyorai, the Medicine Buddha, an especially fitting patron given the plague that inspired the temple's creation.

The original Nara-period pagoda stood seven stories tall, a soaring wooden tower that dominated the Takayama valley. It burned during the Oei period in the late 14th or early 15th century, was reconstructed in 1585, and promptly burned again in the fighting between Kanemori Nagachika and Anegakoji Yoritsuna during their struggle for control of Hida Province. A more modest three-story replacement went up in 1615. That structure too succumbed to fire in 1791 and was rebuilt in 1820 in the form that stands today, the only three-story pagoda in the Hida Takayama region. The Nara-period foundation stone, roughly square with a cylindrical base and a circular hole at its center, survives east of the main hall, a tangible relic of the original 8th-century structure. It has been designated a Takayama City Historic Site.

The current main hall, the Hondo, dates from the mid-Muromachi period, around 1440 to 1462, and is designated a National Important Cultural Property. Inside, wooden statues from the Heian period sit alongside a sword donated by the Ena clan, each artifact a window into a different era of Japanese devotion and power. When Takayama Castle was demolished in 1695 after the Kanamori clan's transfer to Dewa Province, the temple inherited several castle structures, including its main gate. The bell tower gate dates from 1764, housing a bell cast in 1514. Gifu Prefecture has designated additional statues from the Kamakura and Edo periods as tangible cultural properties, making the compact temple grounds a compressed timeline of Japanese religious art spanning nearly a millennium.

The kokubunji system called for both a monastery and a nunnery in each province. The Hida Kokubun-niji, the companion nunnery, stood roughly 900 meters to the west. Its site is now occupied by a Shinto shrine, the physical traces of the Buddhist institution seemingly erased by time. But in 1988, when the shrine underwent renovation, workers uncovered the foundation stones of the nunnery's Kondo, its golden hall. The discovery confirmed the historical record and earned the location a designation as a Takayama City Historic Site. The find is a reminder that beneath Takayama's quiet streets, the footprint of Shomu's 8th-century vision remains embedded in the ground.