Harry Dexter White was born in Boston, Massachusetts, the seventh and youngest child of Jewish Lithuanian immigrants, Joseph Weit and Sarah Magilewski, who had settled in America in 1885. In 1917 he enlisted in the U.S. Army, and was commissioned as lieutenant and served in France in a non-combat capacity in World War I. He did not begin his university studies until age 30, first at Columbia University, then at Stanford University, where he earned a first degree in economics. After completing a Ph.D. in economics at Harvard University at 38 years of age, White taught four years at Lawrence University in Wisconsin.

Senator William Jenner's Interlocking Subversion in Government Departments Investigation by the Senate Internal Security Subcommittee (SISS) looked extensively into the problem of unauthorized and uncontrolled powers exercised by non-elected officials, specifically White. Part of its report looked into the implementation of Roosevelt administration policy in China and was published as the Morgenthau Diary. The report stated,  The concentration of Communist sympathizers in the Treasury Department, and particularly the Division of Monetary Research, is now a matter of record. White was the first director of that division; those who succeeded him in the directorship were Frank Coe and Harold Glasser. Also attached to the Division of Monetary Research were William Ludwig Ullman, Irving Kaplan, and Victor Perlo. White, Coe, Glasser, Kaplan, and Perlo were all identified as participants in the Communist conspiracy ...  The committee also heard testimony by Henry Morgenthau's speechwriter, Jonathan Mitchell, that White had tried to persuade him that the Soviets had developed a system that would supplant capitalism and Christianity.  In 1953, Senator Joseph McCarthy and Eisenhower administration Attorney General Herbert Brownell Jr. revealed that the FBI had warned the Truman administration about White before the President appointed him to the IMF. Brownell made public the FBI's November 8, 1945 letter to the White House warning about White and others, and revealed that the White House had received the FBI report on "Soviet Espionage in the United States," including the White case, six weeks before Truman nominated White to the IMF.  Although he does not dispute that the FBI sent these and other warnings to Truman, Sen. Daniel Patrick Moynihan wrote in his introduction to the 1997 Moynihan Commission report on government secrecy that Truman was never informed of Venona. In support of this, he cited a statement from the official NSA/CIA history of Venona that "no definitive evidence has emerged to show" that Truman was informed of Venona.

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