In the late 1960s, when San Francisco lawyer Frank “Sandy” Tatum and his wife, Barbara, set out to build a family beach home, their vision, for a house that could sleep 12, was large. Their slice of beach on Monterey Bay wasn’t.

Undeterred, the Tatums hired William Turnbull Jr. to design a roughly 1,600-square-foot house on Potbelly Beach in Aptos, Calif., approximately 80 miles south of San Francisco. To maximize the living space, Mr. Turnbull, then just starting what would become a notable architectural career, devised a modern, three-story home anchored by what he called a “sleeping machine,” a white, rectangular structure that housed the bedrooms and bathrooms, said Shelley Tatum Kieran, 60, the youngest of the Tatums’ six children. Two staircases and an open-plan living room with floor-to-ceiling windows flank that core sleeping block.

“It just didn’t look like any other beach house, or any notion of a beach house,” Ms. Kieran said.

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Ms. Kieran said her parents, who led a fairly traditional lifestyle in San Francisco, embraced the design because it fulfilled her mother’s desire for a house filled with light, music and air. Mr. Turnbull, who remained friendly with her parents for years, “let the beach and the water and light do the talking and you were just there to witness it,” she said.

The house is one of 17 homes that comprise the Potbelly Beach Club, a gated community accessible via a private road. The Tatums both died in 2017 and the house is now coming on the market for the first time, asking $6 million, according to real-estate agent Crosby Doe of Crosby Doe Associates, who is marketing the property with Dave Mann of Coldwell Banker Realty. Mr. Mann said homes in the club trade infrequently, but he recently sold a house that is part of the club, located on a bluff above the beach, for about $3.5 million, records show.

Ms. Kieran said her father, an accomplished golfer who was president of the United States Golf Association in the 1970s, banded together with some buddies from Stanford University and others in the 1960s to buy a roughly 5-acre tract of beachfront property that became the beach club. Each beach club member has a share in the partnership and homeowners own their homes; the Tatums’ lot is around ¼ acre with 50 feet of water frontage, records show.

Mr. Turnbull ultimately designed the equivalent of a mini hotel on the site, according to a description of the house in “Buildings in the Landscape,” a 2000 monograph of Mr. Turnbull’s work. He achieved the small footprint by consolidating the bedrooms, bathrooms, kitchen and dining area in what the book described as a narrow “three-story spine” running parallel to the shore, beside which he “saddle-bagged” the living room and staircases under shed roofs, the book said.

The primary bedroom and guest room, connected by a landing with a sink and toilet, are on the second floor. There are two additional bedrooms on the third floor, a girls’ bunk room and a boys’ bunk room, plus a shared bathroom. The only indoor shower is on the first floor; there is a second shower outside. The second-floor bedrooms have barn windows overlooking the living room.

Ms. Kieran recalled that Mr. Turnbull visited the Tatum family’s three-story Victorian house in San Francisco to discuss design details, and he often brought cardboard models of the project.

The architect, who died in 1997, was best known for a design approach closely tied to the specific landscape where a project would be located. One of his best-known projects was Condominium 1, 10 condo units built under a sloping shed roof at the Sea Ranch, a coastal community in Sonoma County that was designed by him and his partners at the firm Moore Lyndon Turnbull Whitaker. Built in the 1960s, the project put him and his collaborators on the map, said Mary Griffin, his widow. Also an architect, Ms. Griffin continued her husband’s firm as Turnbull Griffin Haesloop.

Ms. Griffin said Mr. Turnbull’s designs were heavily influenced by each project’s unique landscape qualities and the Tatums’ house was no exception. “For him, this was not a house designed for some other place,” she said. “It was designed for that place.”

Facing south on Monterey Bay, the site is protected from wind by a cove. The house sits in front of a cliff on the beach. Mr. Turnbull notes in his personal record of the project that to “celebrate” the property’s unusual south-facing view, he installed a window seat in the living room that faces the water. To make the space feel larger, a west-facing glass wall creates an extension of the living area. Meanwhile, a skylight and translucent roofing materials let in sunlight from multiple exposures. “As a result, the building seems a place without shadows,” he wrote.

Completed in 1972, the house appeared on the cover of Architectural Record magazine’s “Record Houses of 1972” issue. The author of a story about the house called its double staircases to the third floor, a local zoning requirement, a “festival of forms” lighted by the translucent roof and a large window.

Ms. Kieran said her family went to the beach every weekend, often with friends. Her mother, an accomplished pianist, brought an upright piano to the third floor and filled the unfinished wood walls throughout the house with books. Because the house is uninsulated, a potbelly stove does most of the heating when it gets cool and, Ms. Kieran said, the house often smells of firewood, salt and sand. “My mother wanted that experience,” she said. “She didn’t want to be insulated from the beach.”

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Ms. Kieran said Mr. Turnbull’s design stood the test of time. Over the years, her parents made few changes, other than adding a first-floor bathroom as they got older, she said. After her parents died, Ms. Kieran and her siblings have shared the house.

“This house was a love letter to my mother from my father,” she said, and the family held a memorial for Barbara Tatum at the house and sprinkled some of her ashes on the beach. Although it is “heartbreaking,” she said, to think of selling the house, she and her siblings knew the day would come when it made sense to put it on the market. “It’s just a lot of responsibility for so many people to carry on,” Ms. Kieran said.

Ms. Griffin said Mr. Turnbull remained friendly with the Tatums until his death. A few weeks before Mr. Turnbull died, the couples were supposed to have dinner, but the plans were canceled due to Mr. Turnbull’s flagging health.

“It’s this tiny, little eccentric house with a big architectural idea,” she said of the Tatums’ beach home. “It was a house he was really proud of.”

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