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He was the Chief of Litigation, Agricultural Adjustment Administration from 1933 to 1935, assistant general counsel of the Works Progress Administration in 1935, chief counsel to Senator Robert La Follette, Jr.'s Committee from 1936 to 1937 and special assistant to the United States Attorney General, 1937 and 1938. In 1948, he worked with the Progressive Party of former Vice President Henry A. Wallace.
Abt was also a member of the Ware Group, a covert organization of Communist Party operatives within the United States government in the 1930s which actively aided Soviet intelligence by passing on government information, as well as furnishing assistance to members of the CPUSA. Abt's sister, Marion Bachrach, was also a member of the group. After the group's founder, Harold Ware, was killed in an automobile collision in 1935, Abt married Jessica Smith, Ware's widow.
In late 1943, Jacob Golos, who headed the CPUSA's secret apparatus, was referred to a spy ring of party members by General Secretary of the party, Earl Browder. This ring had been engaged for some time in espionage for Browder, and held regular clandestine meetings at Abt's apartment. In early 1944, Golos sent Elizabeth Bentley to make contact with the group at Abt's apartment. In attendance was Abt, Victor Perlo, Charles Kramer, Harry Magdoff and Edward Fitzgerald. They discussed paying party dues to Bentley, the various types of information each would be able to deliver, and the type of information other members not in attendance would also be willing to deliver.
In late 1943, the Federal Bureau of Investigation opened an investigation of Abt. Its surveillance showed frequent meetings in the early months of 1944 between Abt and a man then known as Alexander Stevens, one of the several pseudonyms used by the shadowy J. Peters, a party 'enforcer' who at one time headed the CPUSA's secret apparatus, and was involved in clandestine Soviet intelligence activities in the U.S., until his deportation to Hungary in 1948.
In 1946, Abt was nominated by the American Labor state convention to run for the New York Court of Appeals, but the American Labor nominations were soon withdrawn in favor of an endorsement of the Democratic ticket.
In January 1955 Abt defended Claude Lightfoot in Chicago, an African-American Communist on trial under the 1940 Smith Act for belonging to a group that advocates the overthrow of the US government. This trial marked the first time the government attempted to convict an individual solely as a member of a group conspiring against the nation, rather than for individual actions. Although Abt's short and simple defense did not succeed at this trial, Lightfoot's conviction was ultimately overturned by the US Supreme Court in 1964.
During Lee Harvey Oswald's interrogation by the Dallas Police on the evening of 22 November 1963, pending his arraignment for the assassination of President John F. Kennedy, he requested the services of Mr. Abt:
"I want that attorney in New York, Mr. Abt. I don't know him personally but I know about a case that he handled some years ago, where he represented the people who had violated the Smith Act, [which made it illegal to teach or advocate the violent overthrow of the U.S. government] . . . I don't know him personally, but that is the attorney I want. . . . If I can't get him, then I may get the American Civil Liberties Union to send me an attorney."
However, Abt and his wife had left New York City that day for a weekend at their cabin in Connecticut. He did not learn of Oswald's request until the following day. He told reporters that he had received no request either from Oswald or from anyone on his behalf to represent him, and so was in no position to give a definite answer. He said later that "if I were requested to represent him, I felt that it would probably be difficult, if not impossible, for me to do so because of my commitments to other clients." in 1965, the Supreme Court ruled that individuals may invoke their constitutional privilege against self-incrimination and refuse to register with the Government as members of the US Communist Party. Abt considered this decision as his greatest legal victory. Abt was one of the first attorneys to represent Angela Davis for her alleged involvement in the 1970 Marin County courthouse incident.
- KGB agent & Earl Browder instruct Bentley on new recruits, Venona 687 New York to Moscow, 13 May 1944.
- Testimony of John J. Abt, Warren Commission Hearings, vol. 10, p. 116.
- Abt, John; Myerson, Michael (1993). Advocate and Activist: Memoirs of an American Communist Lawyer. Urbana, Illinois: University of Illinois Press. ISBN 9780252020308.
- John Earl Haynes and Harvey Klehr, Venona: Decoding Soviet Espionage in America, Yale University Press, 1999. ISBN 0-300-08462-5.
- Allen Weinstein and Alexander Vassiliev, The Haunted Wood: Soviet Espionage in America - The Stalin Era (New York: Random House, 1999).
- New York FBI report, 9 April 1944, John Jacob Abt FBI file 100-236194, serial 6.
- The Warren Commission Report, Volume X - Testimony of John J. Abt 
- John J. Abt and Michael Myerson, "Advocate and Activist: Memoirs of an American Communist Lawyer," University of Illinois Press (November 1993), ISBN 0-252-02030-8