Jacqueline Kennedy Onassis’ Cape Cod retreat has come up on the open market. It is the first time that the estate known as Red Gate Farm has been offered for sale.

Onassis purchased the expansive slice of Martha’s Vineyard in the late 1970s, commissioning Bunny Mellon—who designed the rose garden at ‘Camelot’—to landscape the property. The house and guest house were designed by Hugh Newell Jacobson and completed in 1981; the main house was revised and expanded in 2000 by Caroline Kennedy. It has remained in the family until the present day.

The grounds occupy 340 acres in a private corner of Martha’s Vineyard, and are anchored by a main house that measures a little more than 6,450 square feet and is designed in the Cape Cod style. The exterior of the home is clad in weathered cedar shingles.

The home’s interior features open, entertainment-ready shared living spaces; ocean views are a constant. The design style is simple, a straightforward approach that doesn’t attempt to compete with the magnificence of the setting.

If there’s a microcosmic piece of New England that represents an ideal of the region, the acreage certainly qualifies. Beaches that stretch into the distance, meadows, forest, stone walls, a blueberry patch, sand dunes, a vegetable garden, tennis court, caretaker’s house, barn, a pair of garages—one sporting an in-law apartment—and the original hunting cabin that was the sole structural occupant of the property at the time of Ms. Onassis’ purchase are among the highlights of this globally singular property.