The Chrysler Museum opened in 1933 as the Norfolk Museum of Arts and Sciences - a modest civic institution typical of Depression-era American cities. Then in 1971, Walter P. Chrysler Jr., son of the Chrysler Corporation founder, donated most of his vast art collection to the museum. His wife, Jean Outland Chrysler, was a Norfolk native, and that connection brought the works home. The gift was transformative. Overnight, Norfolk's small civic museum became one of the major art museums in the Southeastern United States, with holdings to rival institutions in larger cities. The museum was renamed in his honor. Today, the collection has grown to over 35,000 objects, and Russell's hyperbolic line about other museums killing for it is, when you walk the galleries, surprisingly defensible.

The Chrysler holds the Bust of the Savior, a marble bust of Jesus Christ that Bernini created circa 1679 and left in his will to Queen Christina of Sweden. It is widely considered the Baroque master's final sculpture, completed late in his life when he turned from public commissions to personal religious work. Christina treasured it; after her death it passed through Roman collections before Walter P. Chrysler Jr. acquired it and donated it to the museum. Multiple versions of the bust survive and scholars continue to debate which is the primary autograph work - at a 2017 exhibition in Rome the Chrysler bust was compared beside a version from San Sebastiano fuori le mura, and the unfinished drillwork in the Chrysler version's beard, a characteristic Bernini technique, has led many scholars to favor the Chrysler version as the master's own hand. It now sits in the museum's collection as one of the most important Baroque sculptures in the United States. Around it: works by Tintoretto, Veronese, Peter Paul Rubens, Gauthier de Campes, Diego Velazquez, and Salvator Rosa. American galleries hold John Singleton Copley, Thomas Cole, Edward Hopper, Jackson Pollock, Andy Warhol, Richard Diebenkorn, Franz Kline. French rooms hold Delacroix, Manet, Cezanne, Gauguin, Matisse, Braque, and Rodin.

The Chrysler's glass collection is one of the world's greatest - more than 10,000 objects, including outstanding works by Louis Comfort Tiffany. To complement the collection, the museum opened the Perry Glass Studio in 2011, an adjacent 9,200-square-foot working glass facility offering daily glassmaking demonstrations and hosting visiting artists and students. In June 2022, the museum broke ground on an expansion that tripled the studio's size and doubled the number of classes available. Construction concluded in early 2025. The $55 million capital campaign that funded the expansion was supported by the city of Norfolk and the Commonwealth of Virginia. Inside the studio, glassblowers gather molten gathers from the furnace, shape vessels on the marver, twist canes of color into rods that can be pulled into millefiori - all the slow, hot, dangerous work of glass made visible behind safety glass that lets visitors watch from inches away. The studio runs a visiting artist series and an assistantship program for emerging glass artists.

Five blocks east of the main museum, the Moses Myers House preserves the life of a prosperous Jewish merchant in early-19th-century Norfolk. Moses Myers moved to the city in 1787 with his wife Eliza and purchased the lot in 1792. He built a two-story Federal-style brick townhouse. In 1796, Benjamin H. Latrobe is thought to have designed a two-story octagonal wing on the rear to contain a large dining room. The house retains seventy percent of its original contents - American, English, and French furniture, glass, silver, ceramics, and portraits by Gilbert Stuart, Thomas Sully, and John Wesley Jarvis, all commissioned or acquired by the Myers family themselves. Few American historic houses can claim that level of object continuity. The house was listed on the National Register of Historic Places in 1970 and now operates as part of the Chrysler Museum's campus.

The Jean Outland Chrysler Library, named for Walter's wife, holds material on the history of world art with special emphasis on the museum's permanent collection. In 1977, it acquired the library of M. Knoedler & Co., a London art dealer - major historical reference volumes, periodicals, and rare annotated sales catalogs. Among the holdings is the original copy of Mark Twain's speech delivered at the Jamestown Tricentennial Exposition in 1907 - the same Norfolk-area celebration that brought Queen Elizabeth II's predecessors' fascination with American history into focus a half-century later. The library is now physically housed at Old Dominion University, with reading-room access still available at the Chrysler. More than 60,000 schoolchildren from Hampton Roads schools tour the museum each year, guided by about 100 volunteer docents who go through a rigorous year-long training program. The Wounded Indian, a sculpture by Peter Stephenson that the Massachusetts Charitable Mechanic Association believed had been destroyed in the 1950s, turned up here in 1999. A 2020 agreement updated the work's provenance to include the Association's original ownership.