Bishop had originally intended the museum to house family heirlooms passed down to him through the royal lineage of his wife.

The museum was built on the original boys' campus of Kamehameha Schools, an institution created at the bequest of the Princess, to benefit native Hawaiian children; she gave details in her last will and testament.

Hawaiian Hall is home to a complete sperm-whale skeleton, accompanied by a papier-mâché body suspended above the central gallery.

Bottles, crates, and boxes were stowed below, along with gallons of preservatives for insects and plant specimens for the Bishop Museum.

Dedicated on January 13, 1990, Castle Memorial Building houses all the major traveling exhibits that come to the Bishop Museum from institutions around the world.

The archives hold the results of extensive studies done by museum staff in the Pacific Basin, as well as manuscripts, photographs, artwork, oral histories, commercial sound recordings and maps.

When Bishop Museum opened to the public in June 1891, its library consisted of but a few shelves of books in what is today the Picture Gallery.

The book collection consists of approximately 50,000 volumes with an emphasis on the cultural and natural history of Hawaiʻi and the Pacific, with subject strengths in anthropology, music, botany, entomology, and zoology.

Also on the campus is Pauahi Hall, home to the J. Linsley Gressit Center for Research in Entomology, which houses some 14 million prepared specimens of insects and related arthropods, including over 16,500 primary types.

Since 1920, the Secretariat of the Pacific Science Association (PSA), founded that year as an independent regional, non-governmental, scholarly organization, has been based at Bishop Museum.

From 1968 until September 2008, the Bishop Museum owned the Falls of Clyde, the oldest sail-driven oil tanker, which was moored at the Hawaiʻi Maritime Center.