Chambers died of a heart attack on July 9, 1961, at his 300-acre (1.2 km2) farm in Westminster, Maryland. He had suffered from angina since the age of 38 and had had several heart attacks previously.
Cold Friday, his second memoir, was published posthumously in 1964 with the help of Duncan Norton-Taylor. The book prophetically predicted that the fall of Communism would start in the satellite states surrounding the Soviet Union in Eastern Europe. A collection of his correspondence with William F. Buckley, Jr., Odyssey of a Friend, was published in 1968; a collection of his journalism—including several of his Time and National Review writings, was published in 1989 as Ghosts on the Roof: Selected Journalism of Whittaker Chambers.
Chambers's book Witness is on the reading lists of the Heritage Foundation, The Weekly Standard, The Leadership Institute, and the Russell Kirk Center for Cultural Renewal. He is regularly cited by conservative writers such as Heritage's president Edwin Feulner.
In 1984, President Ronald Reagan posthumously awarded Chambers the Presidential Medal of Freedom, for his contribution to "the century's epic struggle between freedom and totalitarianism". In 1988, Interior Secretary Donald P. Hodel granted national landmark status to the Pipe Creek Farm. In 2001, members of the George W. Bush Administration held a private ceremony to commemorate the hundredth anniversary of Chambers's birth. Speakers included William F. Buckley, Jr.
In 2007, John Chambers revealed that a library containing his father's papers should open in 2008 on the Chambers farm in Maryland. He indicated that the facility will be available to all scholars and that a separate library, rather than one within an established university, is needed to guarantee open access.
On 6 January 2010, the Medfield farmhouse at Pipe Creek Farm, in which Whittaker Chambers wrote Witness, was severely damaged by a fire that began in an electrical panel at the front entrance of the home.
In 2011, author Elena Maria Vidal interviewed David Chambers about his grandfather's legacy. Versions of the interview were published in the National Observer and The American Conservative.