Officially opened in 1936, the National Art Gallery occupies the first floor of the National Art Gallery and Dominion Museum building, the ground floor housing the museum collections. Symmetrically opposite the main entrance to the gallery, through the sculpture hall, is the identical entrance to the Gallery of the New Zealand Academy of Fine Arts. The relationship between these two institutions is frequently misunderstood.

In 1936 the New Zealand Academy, a prime mover in the foundation of a National Art Gallery, sold its own gallery in Whitmore Street and devoted the proceeds of the sale, its art collection, and its building fund to the National Gallery. In return it was granted accommodation in perpetuity within the Gallery. The Academy remains, however, a distinct and separate institution. The National Art Gallery and Dominion Museum Act 1930 confirmed previous legislation and constituted the present administration by a board of trustees with separate management committees for the National Art Gallery and Dominion Museum.

Finance is provided by annual grants from the Government and from the Wellington City Council, the Wellington Harbour Board, the Lower Hutt City Council, and other adjacent local bodies. Works of art are purchased from the Sir Harold Beauchamp and T. Lindsay Buick bequests, grants from the Government, and the Wellington City Council and, from time to time, from the T. G. Macarthy Trust. The largest grant, £1,000, is made by the Wellington City Council.

The main collection is confined to contemporary paintings, drawings, and sculpture by British and foreign, and by New Zealand and Australian artists. Separate categories include the Sir Harold Beauchamp, T. Lindsay Buick, Archdeacon Smythe, N. Chevalier, J. C. Richmond and William Swainson collections. The Gallery is particularly rich in graphic art, thanks to gift collections from Bishop Monrad, Sir John Ilott, and Rex Nan Kivell.

The Gallery arranges the itinerary of numerous loan exhibitions from overseas, maintains an active educational programme and, from 1950 till 1960, administered the National Gallery Travelling Scholarship in October. Eru D. Gore was secretary-manager from 1936 till his death in 1948 when S. B. Maclennan was appointed the first director. This was the first appointment in New Zealand of a full-time art gallery director.