The precise date of the shrine is uncertain, but it is generally placed around the middle of the seventh century. A terminus ante quem is provided by the first documentary evidence for its existence, an inventory in
temple records dating to 747, which includes "two items taking the form of a palace building, one with a design of a Thousand Buddhas in repoussé metalwork" (宮殿像弐具 一具金埿押出千佛像), understood to refer to the Tamamushi Shrine, the other being the later Tachibana Shrine. A fuller description is given by the monk Kenshin in his account of the 1230s or 40s of Shōtoku Taishi, prince, regent, culture hero closely associated with the early promotion of Buddhism in Japan, and founder of the temple. He refers to the shrine's tamamushi wings and states that originally it belonged to Empress Suiko (d. 628). Fenollosa, who helped implement the 1871 Plan for the Preservation of Ancient Artifacts through nationwide survey, concluded that it was presented to the Japanese Empress in the 590s. Japanese scholar Uehara Kazu, who has written twenty-eight articles about the shrine over the course of nearly four decades and authored an extensive monograph, has conducted comparative analyses of architectural features and decorative motifs such as the tiny niches in which the Thousand Buddhas are seated. Based on such considerations, the shrine is now dated either to c.650 or to the second quarter of the seventh century.
Perhaps originally housed elsewhere, the shrine escaped the 670 Hōryū-ji fire. Early accounts of the temple and its treasures see it placed on the great altar of the kondō. Kenshin in the early Kamakura period mentions that it faced the east door and that its original Amida triad had at some point been stolen. The shrine was still standing on the altar when Fenollosa was writing early in the twentieth century and is located there also in Soper's studies of 1942 and 1958. Ernest Fenollosa describes the shrine along with the statue he uncovered at Hōryū-ji known as the
Yumedono Kannon as "two great monuments of sixth-century Corean Art". It is referred to by the authors of The Cambridge History of Japan as one of the "great works of Asuka art created by foreign priests and preserved as Japanese national treasures". Domestic production under foreign influence is now the received wisdom.
Evidently it escaped the major fire in the kondō on 26 January 1949 - the building was undergoing dismantling for restoration at the time and all portable items had already been removed. (The damage to Hōryū-ji's celebrated wall paintings led to an overhaul of legislation relating to the preservation of the Cultural Properties of Japan.) The shrine's shibi had already been detached, placed in the treasure hall, and replaced with copies. Today the Tamamushi Shrine is exhibited in the temple's Great Treasure House.