In 1976, the new building, designed by renowned Canadian architect Arthur Erickson, opened under new director Michael M. Ames, who served from 1974 to 1997.

Walter and Marianne Koerner's 1975 donation of their extensive collection of Northwest Coast First Nations art to the museum formed a large part of the building's contents.

On March 9, 1999, Canada Post issued a stamp commemorating the Museum, designed by Barbara Hodgson, based on photographs by William McLennan and Jacqueline Gijssen, and prominently featuring the sculpture The Raven and the First Men by Bill Reid.

The Arthur Erickson's building was designed in 1976, inspired by the post-and-beam architecture of northern Northwest Coast First Nations people.

Other enhancements included MOA's new Multiversity Galleries, the creation of the RRN (Reciprocal Research Network) linking Northwest Coast collections around the world, a relocated and expanded Museum Shop, year-round cafe, and courtyard and outdoor 'events pad' suitable for facility rentals.

Pools had been installed temporarily three times in MOA's history: for a movie shoot in 1993, for the APEC leaders’ summit in 1997, and to celebrate Arthur Erickson's 80th birthday in June 2004.

Designed by Stantec Architecture, the new gallery was converted from the former Michael M. Ames Theatre, and was funded by Montreal-based collector Elspeth McConnell, a $3-million donation from the Doggone Foundation, and a $500,000 grant from the federal government as part of the Canada 150 Community Infrastructure Program.

The museum also has a small wing dedicated to European ceramic art works collected by the late Walter Koerner.

Other notable Bill Reid works include his Bear and Wasco (Sea Wolf) sculptures, some of his gold jewellery, and a prototype of the Haida dugout canoe he carved for Expo 86.

There are many fragments of totem poles from Haida and other First Nations villages along British Columbia's coast in the museum's Great Hall.

The collection includes masks, Yoruba thorn carvings, over 100 Makonde figures from Tanzania, approximately 100 Asante gold weights, weaponry from South Africa and about 100 mortuary objects from Egypt.

Other collections include 2300 Chinese coins and amulets, 200 Sichuan blue thread embroideries dating to circa 1900, rare Tibetan robes, and masks from Noe (Japan), Sunni and Kolam (Sri Lanka), and Pongsan and Yangju (Korea).

The Haida houses outside the museum were built under the direction of Bill Reid, who carved, with Doug Cranmer, many of the totem poles surrounding them.

The Museum of Anthropology works with the Irving K. Barber Learning Centre and others to support the Indigitization program, which provides funding and training for Indigenous communities and organizations to digitize cultural heritage materials.