The museum is named for Thomas Gilcrease, an oil man and avid art collector, who began the collection.

At the turn of the 20th century the federal government allotted lands collectively held by American Indian tribes to private citizens.

Gilcrease purchased his first oil painting titled Rural Courtship by Daniel Ridgway Knight in 1912 for $1,500, but most of the collection was amassed after 1939.

In addition, Gilcrease committed oil property revenue to Tulsa for assistance in maintaining the museum until the $2.25 million bond was fully repaid.

Also on display at the Gilcrease Museum are works by Charles Marion Russell, Alexandre Hogue, and John James Audubon.

Currently, the museum owns about 10,000 pieces of art, including 18 of the 22 bronze sculptures that were created by Frederic Remington.

The collections comprise 300,000 artifacts, covering prehistoric and historic archaeology and ethnographic materials from Native American, Hispanic, pre-Columbian, and Anglo-American cultural traditions.

Gilcrease Museum has one of the most important collections of pre-Columbian projectile points (arrow and spear heads) in North America, and has become a resource that is regularly consulted by archaeologists.

The museum also has a research facility containing sliding glass display shelves for artifacts and a computer database system to help find various pieces.

The secured connector passage between the Reading Room and the document storage area was inspired by the "Vasari Corridor" in Florence, Italy.

The same structure that contains the Reading Room also contains the Great Hall, which is used for many purposes, such as fund raising events, conferences, and short-term gallery displays.

The center was designed by Hastings & Chivetta, completed in 2014, contains 32,000 square feet (3,000 m2) of space and cost approximately $14 million to construct.

Voters approved an 0.6 percent sales tax (known as Vision 2025) on April 5, 2016,[7] which proposed to allocate $65 million for a major expansion/improvement program of Gilcrease Museum.