Johnson designed the interior of the guest house with a living and dining room facing 52nd Street, as well as a bedroom in the rear.

The house was constructed from 1949 to 1950 and initially hosted many functions for the Museum of Modern Art (MoMA), for which Blanchette Rockefeller was a patron.

[5] When the Rockefeller Guest House was commissioned, Johnson was not yet a licensed architect in New York state, but he was already a noted proponent of the International Style of architecture.

[4][14][15] According to Johnson, he built the second floor only to give the impression of height, since he felt "there is no point to doing a one-story house in New York—it would look all wrong".

"[16] The interior arrangement was patterned after Ludwig Mies van der Rohe's unbuilt designs for "court houses" in the 1930s.

[11] The roof of the guest house has a metal fence, which runs from west to east and is slightly set behind the roofline on 52nd Street.

[15][17][23] The plaster was removed from the existing brick walls, which were then painted white, serving as a background for the collection of the house's patron, Blanchette Ferry Rockefeller.

Blanchette then became a patron of the Museum of Modern Art (MoMA), which had been cofounded by Abby Aldrich Rockefeller, her mother-in-law.

[33][34] By the 1940s, Blanchette and John III lived at One Beekman Place in Turtle Bay, several blocks from the Rockefeller Guest House.

[35][36] Abby's and Blanchette's enthusiasm for modern art was not shared by either John III or his father John D. Rockefeller Jr.[27][35] While Abby had converted the top floor at her house at 10 West 54th Street[a] into a private salon, Blanchette wanted a standalone structure for displaying artwork and receiving guests.

[35] Philip Johnson, who was the unofficial architect for MoMA during his career,[38][39][40] also happened to live in Turtle Bay, having resided there for over three decades since at least 1930.

[38] The Empire Mortgage Company, agent for the Rockefeller family, purchased the 25-by-100-foot lot at 242 East 52nd Street in June 1948.

Blanchette and John III intended to continue residing at One Beekman Place and, according to a Rockefeller family spokesperson, they wished to call the structure an "adjunct" rather than a guesthouse.

[19] According to the North American Newspaper Alliance, the guest house "precludes any Elks' convention type of invasion by the 47 Hookers and 48 Rockefellers who were listed as attending the couple's wedding in 1932".

[11][15] The public was first invited to enter the house in 1954, when an exhibition of young artists' work was displayed to benefit MoMA's Junior Council.

[45] The guest house was informally used as an extension of MoMA's operations, hosting parties as well as staff and trustee committees.

[4][46] John Rockefeller III attended several of the parties and once stayed overnight with the couple's children,[b] even though he did not like modern art.

John III came to express remorse over letting Blanchette spend so much time operating the guest house.

The sale was not publicized until February 1964, when The New York Times reported that the Leonhardt family planned to move into the house in May.

Johnson repainted the walls from green to white, removed the original goat's hair curtains, and bought movable furniture.

In addition, the couple put up contemporary works by artists like John Chamberlain, Roy Lichtenstein, and Frank Stella.

According to Symes's friend Christo Michailidis, they had "fallen in love" with the house and found it to be a good place for storing their Art Deco furniture collection.

[52] Symes furnished the guest house with works by Pierre Legrain, Eileen Gray, and Émile-Jacques Ruhlmann.

The auction drew nine bidders, including one who was crossing the Holland Tunnel while placing his bid and found that the house was already sold when he emerged.

[4] By 1996, architect Robert A. M. Stern had suggested that the Rockefeller Guest House was a viable candidate for official landmark status.

[56] Lauder sold the house in December 2023 for an estimated $20 million to Ludo USA, a limited liability company.

[57][58] The Rockefeller Guest House was covered extensively in media such as Architectural Review, Interiors, and The New York Times when it was completed.

[11][53] House and Home magazine, in 1955, described the living room as a "masterpiece of restraint", which in its understated form helped to show off John III's wealth.

[28] According to Russell Lynes, a historian for MoMA, the garden may have been included to cater to the "Rockefellers' taste for things Japanese".