Jeremy Parker and Jiminie Ha, longtime friends and collaborators, knew they had to act fast on a listing about five years ago for a Philip Johnson-designed house in Newburgh, N.Y.

“We were shocked to find this house,” Mr. Parker said in an email. “Nobody knew about a Philip Johnson home in Newburgh,” Ms. Ha added.

The two were interested in buying it together as an investment but had some initial doubts about its authenticity — until inspecting the place in person.

“The bones were there,” Ms. Ha said. But the boxy, two-story house, perched atop a sloping hill, was in disrepair and previous owners had made design changes not in keeping with its midcentury-modern aesthetic. Known as the Wolfhouse, the structure was built in the late 1940s, around the same time as Johnson’s Glass House in New Canaan, Conn. (Johnson designed 25 houses during his career, one of which has since been demolished, according to a spokeswoman for the Glass House museum.)

Fearing Wolfhouse, which sits on 1.4 acres facing the Hudson River, might also be torn down and rebuilt by the next owner, Mr. Parker and Ms. Ha quickly purchased it, paying $650,000. They then spent the next four years and around $1 million more on restorations. The house has since been used for art and cultural events, as well as rented out for short-term stays.

But now with both Ms. Ha, a creative director, and Mr. Parker, a design studio owner, working abroad — he on a preservation project in Tuscany, Italy, and she at the Paris branch of her branding agency — the house is back on the market. The asking price is $2.9 million, with $17,094 in annual property taxes, according to Esteban Gomez of Compass, who is listing the property with his colleague Melissa Marcogliese. “It’s an architectural gem,” Mr. Gomez, who specializes in historic homes, said, describing the quirky house as “essentially two boxes that are stacked atop one another.”

“These homes are sought after because there are so few of them,” he said. “This is part of our architectural history.”

Wolfhouse was commissioned by Benjamin and Ruth Wolf, prominent business owners in Newburgh who had favored Johnson’s signature open-plan designs and integration with the outdoors. The house has 4,018 square feet of interior space, with four bedrooms and three full bathrooms, along with abundant light and expansive vistas of the Hudson and surrounding community from its walls of windows. Light also pours in from windows on the clerestory roof.

Mr. Parker and Ms. Ha worked with original floor plans on file at Columbia University’s Avery Architecture & Fine Arts Library and also received help from the Wolf family, who verified the accuracy of the restoration by providing film footage of the home under construction, archives of photographs and newspaper clippings.

“As preservationists with backgrounds in design and architecture, we felt it was our responsibility to revive the house as it was originally presented,” said Mr. Parker, who has worked on several other restorations.

Some of the many projects he and Ms. Ha undertook at Wolfhouse included replacing the exterior facade, which they said was painted “gender-reveal blue,” with new Cypress wood siding; repairing and upgrading the roof; removing a second-floor deck; resurfacing the original pine floors; and redoing the bathrooms and ’90s-style kitchen.

The two took some contemporary liberties with “the reinterpretation of the kitchen,” said Ms. Ha, who once served as senior director of graphic design at the Guggenheim Museum. The redone kitchen, with high-end appliances, was a collaboration with the Swiss furniture company USM Modular and incorporated steel and wood components, “typical materials used in midcentury kitchens,” Ms. Ha said.

Other modern touches were added to the property, like radiant floor heat on the terra-cotta-tiled ground level, a new French drain and HVAC system, as well as extensive landscaping.

“The property was overrun by invasive wild grape vines, which were killing the trees,” Ms. Ha said.

The house is entered on the ground level through a central foyer that connects to a two-car garage. A hallway leads to a bedroom with an en suite bathroom. There is also a laundry room and storage space.

A staircase in the foyer leads up to the main floor. At one side is an enormous great room with a centrally located brick wood-burning fireplace and areas carved out for lounging and dining, as well as the kitchen. At the other end is the primary bedroom with an en suite tiled bathroom, two additional bedrooms and another bathroom.

Sliding glass doors in the main bedroom and great room open to a covered balcony that looks out onto the Hudson.

Throughout the house are salvaged architectural pieces such as sinks, tubs, and moldings, along with vintage furnishings. These include Jean Prouvé chaise longues, Wassily chairs, a Ronan and Erwan Bouroullec dining table, and a George Nelson coffee table. (Furnishings are also available for sale.)

Like the fireplace, all the glass windows, doors and numerous built-ins are original, while the countertops in the kitchen are made of recycled compressed paper, known as paperstone.

“We hope that there is enough interest in the home’s new rehab, restoration and history that it will go into the right hands,” Ms. Ha said of the next owners.

Whoever purchases it will undoubtedly be taking on more than mere homeownership. “When you buy a home like this,” Mr. Gomez said, “you are automatically part of a very special club of caretakers of these architectural gems.”