The museum exists largely because one woman insisted it should. Florence S. Jacobsen served as a church curator and as general president of the Young Women organization. She championed the creation of a dedicated space to preserve and display the artifacts of her faith. On April 4, 1984, her vision materialized as 63,500 square feet of exhibition space opened to the public. Early visitors encountered the Mormon Panorama, 22 historic paintings by Danish convert C.C.A. Christensen depicting scenes from early church history, alongside contemporary works by living Latter-day Saint artists. Admission has always been free.

The museum closed in October 2014 for a yearlong transformation. When it reopened in September 2015, visitors could step into a specially constructed 220-degree theater that transports them to a thicket of trees in upstate New York. This immersive experience recreates the Sacred Grove where Joseph Smith reported his first vision of God and Christ. A replica of the Newel K. Whitney Store, where Smith received many revelations, allows visitors to walk through a reconstructed piece of early church architecture. Nearby, a wooden chair built by carpenter Brigham Young before his 1832 baptism reminds visitors that even church presidents had ordinary beginnings.

Since 1987, the museum has hosted an International Art Competition founded by Richard Oman. Every three to four years, artists from around the world submit works exploring church and gospel themes across all mediums. The 11th competition in 2019 drew 947 submissions, from which judges selected 151 artists representing 26 countries. Winners see their work purchased for the permanent collection or receive awards of merit. The competition has built a global artistic community united by faith, with pieces ranging from traditional oil paintings to contemporary installations, each offering a different cultural lens on shared beliefs.

In 2013, the museum mounted an exhibition marking the centennial of the Boy Scouts of America with 23 paintings by Norman Rockwell. The collaboration reflected a century-long partnership between the LDS Church and scouting, a relationship that would end in 2018 when the church announced its departure from the program. Those Rockwell paintings, with their idealized visions of American boyhood, captured a moment before that separation. The museum has always documented change as much as tradition, preserving evidence of how the church has evolved alongside American culture.

The Museum Store offers reproductions of works by artists who shaped the visual language of Mormonism: C.C.A. Christensen, John Hafen, Minerva Teichert. Contemporary artists like Walter Rane, Robert Barrett, and Arnold Friberg carry that tradition forward. Beyond art, the store sells historical toys, pioneer-era clothing, and religious literature. A volunteer workforce drawn from surrounding Latter-day Saint communities conducts tours and runs programs, making the museum as much a community gathering place as a repository of artifacts. The building closed briefly in 2020 during the pandemic, but reopened to continue its mission of making two centuries of church history accessible to anyone who walks through its doors.