Disillusioned by the costs of construction and maintenance, Barnsdall donated the house to the city of Los Angeles in 1927 under the stipulation that a fifteen-year lease be given to the California Art Club for its headquarters. The club was there until 1942 when the house was almost demolished. The house has been used as an art gallery and as a United Service Organizations (USO) facility over the years. Beginning in 1974, the city sponsored a series of restorations, but the structure was damaged in the 1994 Northridge earthquake. It was again restored.

The U.S. Department of the Interior designated Hollyhock House a National Historic Landmark in 2007. It was the seventh site in the city of Los Angeles to receive that designation. The house was included in a list of all-time "top ten" Los Angeles houses in a Los Angeles Times survey of experts in December 2008.

In 2005, Project Restore, a non-profit organization dedicated "to the historic restoration and preservation of the civic integrity of the City of Los Angeles," initiated a 10-year restoration project. The restoration included work on the building's floor, wood, doors, windows, art stone, and plaster. In January 2015 it was announced that, following the extensive renovations, the house would once again open for tours on 13 February. The 24-hour event drew large crowds through the night, with many waiting in line for over three hours for admittance.

In 2015, the National Park Service submitted the Hollyhock House along with nine other Frank Lloyd Wright properties to a tentative list for designation as a World Heritage Site. Revised proposals were submitted in 2018. Eight properties were ultimately inscribed on the World Heritage List as part of a submission called "The 20th-Century Architecture of Frank Lloyd Wright" in July 2019. When Hollyhock House together with the seven other buildings in the U.S. were added to the UNESCO World Heritage List, it was the first time that modern American architecture had been recognized by that organization.

As with many of Wright's residences, Hollyhock House has an "introverted" exterior with windows that seem hidden from the outside, and is not easy to decode from the outside. The house is arranged around a central courtyard with one side open to form a kind of theatrical stage (never used as such), and a complex system of split levels, steps and roof terraces around that courtyard. The design features exterior walls that are tilted back at 85 degrees (which helps provide a "Mayan" appearance sometimes referred to as the Mayan Revival style), leaded art glass in the windows, a grand fireplace with a large abstract bas-relief, and a moat. Water is meant to flow from a pool in the courtyard through a tunnel to this inside moat, and out again to a fountain. The front doors are stepped similarly to the entryway. The split doors rest on pins and swing open easily despite their massive weight. The keyhole is concealed with a decorative flap.

The hollyhock (Aline Barnsdall's favorite flower) is used as a central theme to the house, with many symmetrical decorations adapting the plant's general appearance. Planters are decorated with the motif and filled with the plants themselves, and Wright's stained glass windows feature a highly stylized hollyhock pattern. An interesting feature is the mitered glass corners at the windows; an early idea Wright later used at Fallingwater. Wright notably referred to the architecture of Hollyhock House as "California Romanza," borrowing from a musical term translating to "freedom to make one's own form."

Hollyhock House features an entertainment room immediately to the right of the entrance. This room contains possibly the first built-in entertainment center, complete with LP-sized cabinets along the floor. Other notable rooms include a child's play area as well as a modernist kitchen, which long housed the museum gift shop.

Like many houses designed by Wright, Hollyhock House proved to be better as an aesthetic work than as a livable dwelling. Water tended to flow over the central lawn and into the living room, and the flat roof terraces were conceived without an understanding of Los Angeles's rains. The cantilevered concrete also did not stand up well to the area's earthquakes. There were a considerable number of revisions. Two smaller structures, called Studio Residences A and B, were built on the grounds. Residence A still stands. Barnsdall also commissioned a private kindergarten which was never built. The property also includes a smaller building designed by modernist architect Richard Neutra.