Rockefeller was born in New York City, New York. He grew up in an eight-story house at 10 West 54th Street, the tallest private residence ever built in the city. Rockefeller was the youngest of six children born to financier John Davison Rockefeller Jr. and socialite Abigail Greene "Abby" Aldrich. John Jr. was the only son of Standard Oil co-founder John Davison Rockefeller Sr. and schoolteacher Laura Celestia "Cettie" Spelman.

Rockefeller traveled widely and met with both foreign rulers and U.S. presidents, beginning with Dwight D. Eisenhower. At times he served as an unofficial emissary on high-level business. Among the foreign leaders he met were Saddam Hussein, Fidel Castro, Nikita Khrushchev, and Mikhail Gorbachev.  In 1968, he declined an offer from his brother Nelson Rockefeller, then governor of New York, to appoint him to Robert F. Kennedy's Senate seat after Kennedy was assassinated in June 1968, a post Nelson also offered to their nephew John Davison "Jay" Rockefeller IV. President Jimmy Carter offered him the position of United States Secretary of the Treasury but he declined.  Rockefeller was criticized for befriending foreign autocrats in order to expand Chase interests in their countries. The New York Times columnist David Brooks wrote in 2002 that Rockefeller "spent his life in the club of the ruling class and was loyal to members of the club, no matter what they did." He noted that Rockefeller had cut profitable deals with "oil-rich dictators", "Soviet party bosses" and "Chinese perpetrators of the Cultural Revolution".  Rockefeller met Henry Kissinger in 1954, when Kissinger was appointed a director of a seminal Council on Foreign Relations study group on nuclear weapons, of which David Rockefeller was a member. He named Kissinger to the board of trustees of the Rockefeller Brothers Fund, and consulted with him frequently, with the subjects including the Chase Bank's interests in Chile and the possibility of the election of Salvador Allende in 1970. Rockefeller supported his "opening of China" initiative in 1971 as it afforded banking opportunities for the Chase Bank.  Though a lifelong Republican and party contributor, he was a member of the moderate "Rockefeller Republicans" that arose out of the political ambitions and public policy stance of his brother Nelson. In 2006 he teamed up with former Goldman Sachs executives and others to form a fund-raising group based in Washington, Republicans Who Care, that supported moderate Republican candidates over more ideological contenders.

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