It has grown into a major art museum with a permanent collection of more than 3,500 works of art from the nineteenth century to the present, including works by such contemporary painters and sculptors such as John Chamberlain, Chuck Close, Eric Fischl, April Gornik, Donald Sultan, Elizabeth Peyton, as well as by masters Dan Flavin, Roy Lichtenstein, Jackson Pollock, Lee Krasner, and Willem de Kooning.

In 1981, further depth was added to the collection when nearly 200 works of art by the prominent American painter, critic, and longtime Southampton resident Fairfield Porter (1907–1975) were donated by his wife Anne and by the artist's estate.

Once home to Jackson Pollock, Willem de Kooning, and Roy Lichtenstein, among many others, today's residents, full-time or seasonal, include Chuck Close, Ross Bleckner, April Gornik, Eric Fischl, Ilya and Emilia Kabakov, and Donald Sultan.

[1] Recognizing the need to grow and to provide for a modern facility with appropriate climate control, the board of trustees decided to embark on a new project to design and construct a purpose-built building.

Inside, the single-floor museum is structured in a very simple way, with public functions (such as reception, store, and café) to the west, administrative offices and art handling to the east, and the galleries, arrayed in two parallel bars, on either side of a central hall.

Not coincidentally, these were the years when Porter lived in Southampton, New York, and in 1979 his estate recognized the bond between the artist and the Museum by donating some 250 works to the Parrish collection.

Porter painted what he was familiar with—his family and friends and the places he lived and visited, including Southampton, New York and a family-owned island off the coast of Maine where he had summered since childhood.

In 1958, Alfred Corning Clark donated to the Parrish more than two dozen paintings and watercolors, among them works by Ralph Blakelock, James A. M. Whistler, William Glackens, and Arthur B. Davies.

In 1961, in addition to artists mentioned previously, Mrs. Littlejohn bequeathed to the Parrish works by John Frederick Kensett, Otis Bullard, E. L. Henry, George Luks, and Everett Shinn, among others.

Since the Porter bequest of 1975, the Parrish has increasingly focused on American painting of the twentieth and twenty-first centuries, with a special emphasis on artists who have maintained studios on the East End of Long Island since the 1950s.

More recent East End arrivals whose work the Museum holds are Chuck Close, Joan Snyder, Joe Zucker, Alice Aycock, Lynda Benglis, April Gornik, Keith Sonnier, Mary Heilmann, Malcolm Morley, and many more.

The collection also includes a substantial number of prints and drawings, among them works by George Bellows, Marsden Hartley, Larry Rivers, Helen Frankenthaler, and Robert Rauschenberg.

In 1982 Paul F. Walter donated drawings by many Minimalist painters and sculptors, including Barry Le Va, Dorothea Rockburne, Mel Bochner, and Jennifer Bartlett.

Robert Dunnigan gave the Museum more than 500 etchings in 1976, with prints by many of the American artists who participated in the “painter-etcher” movement of the late nineteenth century.

Recent solo shows have included Alice Aycock: Some Stories are Worth Repeating; Jennifer Bartlett: History of the Universe—Paintings 1970–2011; Rackstraw Downes: Onsite Paintings, 1972–2008; Alex Katz: Seeing, Drawing, Making; Roy Lichtenstein: American Indian Encounters; Platform: Maya Lin; Platform: Josephine Meckseper; Jean Luc Mylayne; Alan Shields: Stirring the Waters; Michelle Stuart: Drawn from Nature; and Jack Youngerman: Folding Screen Paintings.

[9] Recent shows have focused on Steven and William Ladd; Alan Shields; Jules Feiffer; Joe Zucker; Robert Dash; Chuck Close; and Andreas Gursky.

In an interview for Hamptons Magazine in July, 2012, Sultan said that for the opening in November, 2012, the Parrish would show its first-ever installation featuring art from all periods in the museum's 2,600-work permanent collection, adding that many works will be completely new to visitors.