With a floor area of 14,000 square feet (1,300 m2), it is one of the largest residences designed by Wright, who also called the building the last of his Prairie style houses.

The living room at the center is a domed structure, with clerestory windows on the sides, a central elliptical chimney, and a viewing platform at the top.

It was hosting 100 conferences a year by the 1980s, with meetings focusing on education, family affairs, society, and international relations.

[5][8][9][a] Some parts of the estate are lawns that are mowed frequently, while other sections are left as wild marshland to attract migratory birds.

[7] The estate includes several pieces of sculpture by artists such as David Aronson, Robert Cook, Jose de Creeft, Emilio Greco, Milton Hebald, Berto Lardera, Carl Milles, and Abbott Pattison.

[5][6][19] According to the writer Brendan Gill, this comment was likely facetious, since the architect was known to compliment his own work and then downplay the remark "in seeming modesty".

"[9][25] The floor plan consists of a central octagonal hub, the living room, from which four wings radiate in a pinwheel configuration.

[9][40] The mezzanine extends off one side of the living room, leading to the master bedroom wing;[57][34] it is clad with sculpted oak.

[64] Wright's apprentice Edgar Tafel added a storage vault underneath the mezzanine, allowing him to conceal a support beam.

[11] The east wing, north of the swimming pool, was originally used by the Johnson family's children[57][34] and has a playroom or terrace room.

[30] Johnson owned 50 acres (20 ha) at Wind Point near Lake Michigan,[11] and he and Roach gave Wright a tour of the site in late 1936.

[48] Sam Johnson recalled that, after the family moved to Wind Point, "I thought my friends would never find me, but they would all get on their bikes and come out here and we'd have a wonderful time.

[67] The Johnson family moved out of Wingspread in 1959, relocating to a neighboring house that better reflected Purcell's design ideals.

[89] The Johnson Foundation hosted its first major conference, a Midwest Regional American Assembly meeting, at Wingspread on November 17, 1960.

[93] Most of the house's earliest conferences attracted no more than 75 to 100 attendees,[89] and the foundation had to issue timed-entry tickets for some events due to relatively limited capacity.

[94] During the house's first two years as a conference center, it hosted discussions on such topics as China–United States relations, arms control, and higher education careers.

[96] The conference center's earliest visitors included former U.S. first lady Eleanor Roosevelt; former United Nations General Assembly president Frederick Boland; and poets Archibald MacLeish, Karl Shapiro, and Mark Van Doren.

[9] During a particularly contentious meeting in 1985 that attracted protests,[111] Wingspread's grounds were closed to non-attendees for the first time in the conference center's history.

[114] The living room's roof began to sag by up to 3 inches (76 mm) during 1993 and 1994 after particularly severe winter weather caused ice accumulations.

[39][115] Foundation employees were allowed to continue using their offices in the building, while visitors could use the rooms in each wing, but conferences were moved to an outbuilding called the House.

[61][23] Because the building was listed on the National Register of Historic Places, it was infeasible for workers to remove parts of the roof and add steel beams to replace the existing, weakened ones.

[118] Although carbon fiber had not existed when the house was built, restoration architect Robert Silman decided to use it after a Taliesin director said that Wright would have used the material if it had been invented during his lifetime.

[120][121] Under Gibbons's leadership, the Johnson Foundation began planning the Guest House, a 40-room hotel on the Wingspread campus for conference attendees.

[109][128] The foundation had been established in January 1959 for "charitable, educational or religious purposes", with Leslie Paffrath as its first president[87][88] and Barbara Sargent as its only other employee.

[131][110] The Johnson Foundation has helped plan conferences and meetings at the house, including organizing transportation and lodging for visitors.

[132] Conferences are restricted to a small number of topics, namely education, family affairs, society, and international relations.

[142][143] In the late 20th century, anyone could tour the house if they booked in advance;[144][65] if a conference was taking place, only the grounds were open to the public.

"[148] A 1986 article for the Journal Times said that "nature and structure seem to have been living in perfect harmony" at Wingspread, despite its brick-and-masonry construction.

[110]A writer for the Journal Times said in 1993 that Wingspread and the Johnson Wax Headquarters "overshadow the rest of the architecture in Racine County" because they were so well-known.

[9] A 1994 article in the Journal Times described the house as a tranquil place where "even in the midst of the most heated controversies, opponents may find common ground".