The collection spans from 6,500 BC to 400 AD — Greek, Roman, and Etruscan antiquities arranged not by object type but by theme: Gods and Goddesses, Dionysos and the Theater, Stories of the Trojan War. Among the outstanding pieces is the Victorious Youth, one of the few life-size Greek bronze statues to survive into the modern era. The Lansdowne Heracles is a Hadrianic Roman sculpture in the manner of Lysippus. The Marbury Hall Zeus stands 81 inches tall, recovered from ruins at Tivoli near Rome. Then there is the Getty kouros, which the museum lists as 'Greek, about 530 BC, or modern forgery' — because scientific analysis has been unable to settle the question definitively. If genuine, it is one of only twelve surviving intact lifesize kouroi. The Villa also holds jewelry, coins, and a 20,000-volume library covering art from antiquity.

Getty had opened a small gallery next to his Pacific Palisades home in 1954. The full villa came two decades later, designed by architects Robert E. Langdon Jr. and Ernest C. Wilson Jr. After Getty's death, the museum inherited $661 million and began planning the Getty Center in nearby Brentwood. To accommodate both campuses, the trust split the collections: the antiquities went to the Villa, the rest to the Center. In 1997, the Villa closed for renovation. Architects Rodolfo Machado and Jorge Silvetti redesigned the campus, surrounding the building with landscaping intended to evoke an active archaeological dig. Architectural Record praised the result as 'a near miracle — a museum that elicits no smirks from the art world.' The Villa reopened on January 28, 2006.

There are four gardens at the Getty Villa, planted with species native to the Mediterranean and documented in ancient Roman texts. The Outer Peristyle is an exact proportional replica of the garden at the Villa dei Papiri, with a 220-foot-long pool at its center. Pomegranate trees stand at each corner, surrounded by acanthus, ivy, hellebore, lavender, and iris. The Herb Garden to the west grows fruit trees — pomegranate, fig, apricot, apple, citrus, and pear — bounded by an olive grove on terraces above. Copies of Roman bronzes excavated at the Villa dei Papiri are scattered throughout the grounds. The 64-acre campus sits on a hill about 100 yards from the Pacific Ocean, though the architecture keeps the sea mostly out of view, producing what one critic described as 'a sense of detachment from its immediate environment.'

The Getty's possession of some objects has been disputed by the Italian and Greek governments, who argue that pieces were looted and should be returned to their countries of origin. In 2007, the Getty agreed to return 40 looted items to Italy. In 2022, the Villa served an unusual diplomatic function: President Joe Biden and First Lady Jill Biden hosted Western Hemisphere leaders for dinner there during the 9th Summit of the Americas — a first for the campus. On January 7, 2025, the Palisades Fire reached the villa's grounds, burning roughly 1,400 trees. The structures and the collection were unharmed. The Villa closed for remediation and reopened on June 27, 2025. The Outer Peristyle, the galleries, the kouros of uncertain authenticity — all survived.