The foundations for the present collections were first assembled in the former Museum of the American Indian in New York City, which was established in 1916, and which became part of the Smithsonian in 1989.

[3] In conjunction with this star-studded gala, Retha Walden Gambaro organized an exhibition featuring 120 Native American artists.

[10] The creation of the museum brought together the collections of the George Gustav Heye Center in New York City, founded in 1922, and the Smithsonian Institution.

The current arrangement represented a political compromise between those who wished to keep the Heye Collection in New York, and those who wanted it to be part of the new NMAI in Washington, DC.

Custom House, which was refurbished for this purpose and remains an exhibition site; its building on the Mall in Washington, DC opened on September 21, 2004.

[16][18] As an enrolled member at San Felipe Pueblo, she will be the first Native American woman to serve as a Smithsonian museum director.

[18][20] As of 2023, Greg Sarris serves as the Chairman of the Board of Trustees for the Smithsonian Institution's National Museum of the American Indian.

[21] Kevin Gover was the director of the Smithsonian Institution's National Museum of the American Indian beginning December 2007 until January 2021.

[22] Gover succeeded W. Richard West Jr. (Southern Cheyenne), who was the founding director of the National Museum of the American Indian (1990–2007).

This was official travel funded by the Smithsonian,[23] and many within the Native American community offered defenses of West and his tenure.

The five-story, 250,000-square-foot (23,000 m2), curvilinear building is clad in a golden-colored Kasota limestone designed to evoke natural rock formations shaped by wind and water over thousands of years.

The Heye Foundation's Museum of the American Indian opened to the public on Audubon Terrace in New York City in 1922.

The Heye Center offers a range of exhibitions, film and video screenings, school group programs and living culture presentations throughout the year.

In Suitland, Maryland, the National Museum of the American Indian operates the Cultural Resources Center, an enormous, nautilus-shaped building which houses the collection, a library, and the photo archives.

[33] The national memorial was unveiled with a virtual event on Veterans Day 2020, with a dedication ceremony postponed due to the COVID-19 pandemic in the United States.

[35] The memorial comprises a vertical steel circle standing on a stone drum, surrounded by benches and engravings of the logos of the military branches.

[36] Four stainless steel lances are incorporated around the benches where veterans, family members, tribal leaders, and other visitors can tie cloths for prayers and healing.

[39] The museum has programs in which Native American scholars and artists can view NMAI's collections to enhance their own research and artwork.

[40] The exhibit is built around the Two Row Wampum Treaty, known from both Indian oral tradition and a written document that some believe is a modern forgery.

Two Washington Post writers, Fisher and Richard, expressed "irritation and frustration at the cognitive dissonance they experienced once inside the museum".

[46] For Fisher, the displays did not meet his expectations that they would tell the familiar story of Indians' evolution from prehistory to modern times.

[46] Jacki Thompson Rand, a Choctaw historian who served on the advisory board up to 1994, titled her reflections Why I Can't Visit the National Museum of the American Indian: "The absence of Native knowledge and the consequent inability to effect the required translation undermined exhibitions … Art and material culture were the preferred media for transferring knowledge about Native America to an unknowing audience.