American Folklife Center collections relating to the Indigenous peoples of North, Central, and South America include materials from over 200 tribal communities throughout the United States, Canada, and northern Mexico in addition to materials from other parts of the Americas. Starting with the earliest ethnographic recordings, made in March 1890 by several Passamaquoddy men for the ethnologist Jesse Walter Fewkes, the Library became the home in the 1940s for most of the recordings assembled by linguists, anthropologists, and early ethnomusicologists such as Frances Densmore, John Peabody Harrington, Alice Fletcher, Truman Michelson, and others working for the Smithsonian Institution's Bureau of American Ethnology. The Library also sponsored fieldwork. A partnership between the Library and the Bureau of Indian Affairs supported field trips by Willard Rhodes, a Columbia University music professor, who spent most summers between 1939 and 1952 visiting tribal communities, schools, and events in Oklahoma, the northern Plains, the Northwest Coast, and the Southwest, recording contemporary song genres of the day.

The collections in what was then called the Archive of Folk Song (located within the Library's Music Division) continued to grow as other documentarians and organizations sought a home for field recordings, particularly those made using formats such as wax cylinders and wires that were rapidly becoming obsolete, since the Library had a recording laboratory capable of reformatting and preserving them. This process accelerated after the creation of the American Folklife Center in 1976, the administrative relocation of the Archive into the Center, and the establishment of its Federal Cylinder Project [FCP]. Publicity surrounding the project that focused on the earliest recordings, particularly those from tribal communities, led to the deposit in the Library of recordings originally held in other repositories, thus enriching and broadening the resources.

Since its beginning, the Center has also sponsored public events, some of which have featured tribal speakers and storytellers, musicians and dancers, and has now provided an online home for Living Nations, Living Words, the Native American poetry project of U.S. Poet Laureate Joy Harjo.

The bulk of the documentation here, especially the earlier recordings, consists of songs rather than spoken word. Ethnologists and linguists often took down narratives via dictation, reserving the audio recordings for songs. In many cases, the recordings ended up in different repositories than the written documentation. Some original audio recordings were copied and found in several archives. In those situations, research may require contacts at multiple institutions.

The documentation in the American Folklife Center archive is the intellectual property of the communities of origin. These communities must be consulted for matters of access and use.