It is the largest private contemporary art museum in the United States, holding more than $4.6 billion in net assets, and is noted for its setting in a broad natural landscape.

Its most significant expansion was finished in the late 2010s, with outdoor sculpture installations, landscaping, a new complex designed by Thomas Phifer, and an environmental center being added.

[1] Following a near-death accident on a helicopter trip in Russia, Rales decided to take on a philanthropic project, which became the establishment of a private contemporary art museum.

[2] Built on land that was formerly a fox hunting club, Glenstone is named for the nearby Glen Road, and because of stone quarries located in the vicinity.

Located 15 miles (24 km) from downtown Washington, D.C., the museum's initial 30,000-square-foot (2,800 m2) Modernist limestone gallery opened in 2006 and admitted visitors two days a week.

[11][12] Speaking on Public Radio Tulsa's Museum Confidential program in 2019, curator Emily Wei Rales said that plans do not include substantial expansion, and will likely be limited to "one or two smaller buildings to house artworks, maybe in the woods, maybe on an adjoining property".

[19] In July 2021, Glenstone announced a purpose-built expansion to house Richard Serra's large-scale sculpture Four Rounds: Equal Weight, Unequal Measure (2017) that the museum had acquired from the artist.

[32] In 2018, the introduction of the Pavilions expansion debuted single-artist installations and exhibitions from artists Cy Twombly, Robert Gober, Pipilotti Rist, Charles Ray, On Kawara, Martin Puryear, Michael Heizer, Lygia Pape, Brice Marden.

Other artists who have been on display at Glenstone have included Roni Horn, Alexander Calder, Ruth Asawa, David Hammons, Alighiero Boetti, Kerry James Marshall, Shirin Neshat, Rirkrit Tiravanija, and Mark Rothko.

The museum buildings are located toward the center of the campus, and visitors approach the galleries from gravel parking lots via a pathway through the property that is about one-third mile (0.5 km) long.

[39] The 2018 expansion added 50,000 square feet (4,600 m2) of gallery space in a 204,000-square-foot (19,000 m2) museum structure called the Pavilions, designed by American architect Thomas Phifer.

Mitchell and Emily Wei Rales have mentioned several buildings as particular influences on the design: the Ryoan-ji Zen temple in Kyoto, Japan; the Menil Collection in Houston, Texas; the Beyeler Foundation in Basel, Switzerland; and the Louisiana Museum of Modern Art in Denmark.

[34][6] Regarding the architectural approach to the Pavilions, Emily Rales said, "we knew we wanted these discrete spaces where you could essentially enter into another world that happens to be an art installation".

[44] Pulitzer Prize-winning critic Sebastian Smee wrote of the Water Court:It's as if you've entered a beautiful sanctuary, possibly in another hemisphere, maybe another era.

[47] This outdoor space hosts large art installations by artists including Jeff Koons, Félix Gonzalez-Torres, Michael Heizer, and Richard Serra.

[25] In a review for The Washington Post in 2018, Philip Kennicott wrote that Glenstone is a "must-see" museum and that its creators successfully "integrate art, architecture, and landscape".

Kennicott tempered his review by mentioning that the museum's distinctive architecture and layout continually confront visitors with "strange visions" that will make it "interesting to see how it is received".

He wrote that the museum's collection excels in its focus on conventional paintings, sculptures, and installations but excludes more modern media, such as video or performance art.

"[7] In Washingtonian, Dan Reed praised Glenstone's suburban setting, saying it "has little in common with the crowded downtown art meccas" and describing it as soothing, contemplative, and stunningly landscaped.

He wrote that it "is a huge success on many levels, but among its triumphs is fashioning a mood and space to look intently and even to fall in love with art that most will be disposed to find difficult, forbidding, or inscrutable."