The permanent exhibition unfolds in two independent circuits arranged chronologically and geographically. The first moves through the ancient world: Greco-Roman art from classical antiquity, pieces from the Near East and the Nile Valley, Egyptian and Mesopotamian artifacts, Persian works spanning pre-Islamic and Islamic periods, and Armenian art reflecting Gulbenkian's own heritage. The second circuit covers European art from the 11th century onward. It begins with ivory carvings and illuminated manuscripts, progresses through Renaissance paintings from the Netherlands, Flanders, France, and Italy, and arrives at an extensive collection of French 18th-century decorative arts -- gold and silver objects, furniture by the greatest Parisian ebenistes, paintings, and sculpture. The sequence culminates in a dedicated gallery for Rene Lalique's Art Nouveau jewelry and glass, displayed as the culmination of European decorative achievement.

The list of artists represented reads like a syllabus for European art history: Domenico Ghirlandaio, Rubens, Rembrandt, Rodin, Van Dyck, Degas, Monet, Manet, Turner, Gainsborough, Fragonard, Frans Hals, Renoir, Boucher, Burne-Jones. There are Venetian views by Francesco Guardi, English landscapes by Turner and Gainsborough, sculptures by Houdon and Carpeaux, and furniture by Andre-Charles Boulle -- the French cabinetmaker generally considered the preeminent artist in the field of marquetry. Gulbenkian did not collect schools or movements; he collected individual masterpieces. A Rembrandt self-portrait hangs near a Ghirlandaio portrait, not because they represent their respective periods but because each piece met a single criterion: it had to be the finest available example. The Centro de Arte Moderna, the museum's modern art wing, extends the collection with twelve thousand contemporary works, actively commissioning new pieces to keep the institution's holdings growing.

The museum was purpose-built for Gulbenkian's collection, which made it unusual in the 1960s, when most art museums occupied repurposed palaces or government buildings. Architects Alberto Pessoa, Pedro Cid, and Ruy Jervis d'Athouguia designed a structure that interacts with its surrounding park, itself designed by landscape architects Antonio Viana Barreto and Goncalo Ribeiro Telles. Views into woods and wetlands punctuate the galleries, so that a visitor might turn from a Rembrandt to see sunlight filtering through trees outside the window. Woodland paths offer views back toward the dramatic building, whose edges incorporate terraces and water features that blur the boundary between architecture and landscape. The park occupies a block bordered by the Avenida de Berna to the north and the Centro de Arte Moderna to the south.

In 2024, the Centro de Arte Moderna reopened after a major redevelopment by Japanese architect Kengo Kuma and Associates, a project that cost fifty-eight million euros. The most prominent addition is a hundred-meter-long entrance canopy clad in dark ash planks with handmade white tiles on top, inspired by the Japanese engawa -- the covered transitional space between interior and exterior that is fundamental to traditional Japanese architecture. The architects also relocated the museum's main entrance from north to south, reorienting the visitor's experience. The choice of Kuma -- known for buildings that dissolve the distinction between structure and environment -- extended the museum's founding philosophy into the 21st century. Gulbenkian wanted a museum where art and nature existed in conversation. Kuma's canopy, hovering between the gallery spaces and the parkland, literalizes that ambition in dark wood and white ceramic.