The collection is centered around articles from the Heian and Kamakura periods and includes paintings, calligraphy, sutras, sculpture and Buddhist ritual objects.

Among these are a set of the complete Buddhist canon (issaikyō), writings of Kūkai and Minamoto no Yoritomo, founder of the Kamakura Shogunate, mandalas and portraits of priests.

Following the Meiji Restoration, at the end of the 19th century, the government introduced a policy of separation of Shinto and Buddhism (Shinbutsu bunri) and many Buddhist temples became destitute.

Some of Koyasan's artworks ended up in collections of museums in Tokyo, Kyoto or Nara or were sold to private persons, both domestically and to foreigners.

Construction of the building in a wooded area southwest of Daishi Kyōkai, the administrative center of Shingon Buddhism, was completed on 30 September 1920.

The opening of the museum was celebrated on 15 May 1921 and the head priest of Kongōbu-ji, Hōryū Doki (土宜法龍) assumed the position of first director.

On 1 May 1961, the museum was expanded with the construction of the Koyasan Great Treasury (高野山大宝蔵), at the time the biggest of its kind in Japan and used mainly for nationally designated tangible cultural properties of the fine arts and crafts type.

In 1984, on the 1150th anniversary of Kōbō-Daishi entering the state of eternal meditation (nyūjō (入定)), a new large standalone and fireproof building was constructed to the east of the old structure, effectively doubling the display space.

It also provided the museum with modern features such as proper lighting, full temperature and humidity control; things that are still lacking in the old structure today.

Painted on three hanging scrolls with color on silk, this work dates to around 1200, the turn from the Heian to the Kamakura period and is owned by Yūshi Hachimankō Jūhakkain (有志八幡講十八箇院).

[15][10] Ike no Taiga, among the most famous Edo period painters, decorated fusuma sliding partitions with landscape scenes in the nanga style.

The designated National Treasure known as Landscape and figures on sliding partitions (紙本著色山水人物図, shihon chakushoku sansui jinbutsuzu) consists of ten paintings with color on paper.

An 8th century Tang dynasty Miniature Buddhist shrine (木造諸尊仏龕, mokuzō shoson butsugan) brought back from China by Kūkai is stored at the museum.

[16][8][17] Six of the group of Eight Attendants of Fudō Myōō (木造八大童子立像, mokuzō hachidai dōji ryūzō), the oldest, dating to 1197 Kamakura period by Unkei are National Treasures: Ekō (慧光), Eki (慧喜), Ukubaga (烏倶婆誐), Shōjō Biku (清浄比丘), Kongara (矜羯羅), Seitaka (制多迦).

[8][18][16][17][19] A small Chinese style chest (karabitsu) with maki-e, mother of pearl inlay (澤千鳥螺鈿蒔絵小唐櫃, sawachidori raden makie kokarabitsu) and plover motifs from the 12th century Heian period is the only crafts National Treasure at the museum.

Shōchi-in (正智院) and Hōju-in (宝寿院) own Japanese manuscripts of parts of the Wenguan Cilin (文館詞林, Bunkan shirin, lit.