The early 1940s marked a changing of the guard in the Kennedy clan. Joseph Kennedy, Sr.'s political star was in eclipse–in the country at large, because of his support for appeasement while Ambassador to Great Britain, and in the Democratic party in specific, because of his opposition, in 1940, to Franklin Delano Roosevelt's nomination to run for a historically-unprecedented third term as President of the United States. His children, however, were on the rise. Kathleen Kennedy, JFK's favorite sibling, was working for a newspaper in Washington, and being romanced by the social elite of both the U.S. and Great Britain. Joseph Kennedy, Jr. vigorously opposed U.S. involvement in World War II while at Harvard Law School, but once Pearl Harbor was bombed by the Japanese, he enlisted in the Naval Aviation Cadet Program, and was soon flying missions over Europe. Meanwhile, JFK (now "Ensign Kennedy") was working for Naval Intelligence in Washington, and sleeping with a Danish beauty named Inga Arvad, who worked as a columnist for the same paper as Kathleen. An exotic, well-traveled woman, Inga had connections to Nazi leaders, a circumstance which eventually got JFK in trouble with his superior officers. The young ensign was reassigned to a bureaucratic post in South Carolina, and his romance with the Danish beauty fizzled.

JFK found South Carolina paralyzingly dull, and he begged his father to pull strings to get him assigned to sea duty. Joseph Kennedy, Sr. obliged, and in late 1942, JFK was given an assignment on a Motor Torpedo Boat, or "PT boat," as it was informally known. After six months of training, he and his crewmates shipped out from San Francisco, bound for the South Pacific and combat with the Japanese. Promoted to lieutenant early in 1943, he was given command of a boat designated PT 109, and was the skipper of this boat on the night of August 2, 1943, when it was rammed by the Japanese destroyer Amigari. Two of JFK's crew were killed outright, while the others tried to stay afloat amid the wreckage. Under the young lieutenant's leadership, eleven men, several badly wounded, managed to hang on to the half of the PT boat that was still afloat and wait for help. None came, and after nearly fifteen hours, JFK led the men on a grueling swim to a nearby island. From there, he and his subordinate, Ensign Ross, made various forays through the coral islands, searching for help. It was days before they found a group of natives who carried a message to a British base, some thirty-eight miles away. Finally, on August 7, JFK and the other survivors were rescued by a party of British scouts and carried to safety.

The ordeal made JFK a war hero. He received the Purple Heart, as well as the Navy and Marine Corps Medal, and for the first time in his life, he began to outshine his brother Joe. After the incident of PT 109, however, the rest of JFK's war experience proved somewhat anticlimactic. JFK's frail health gave way: he contracted malaria, and his old back problems flared up. He was rotated back to duty in the U.S., and by spring of 1944, he found himself laid up in Boston's Chelsea Naval Hospital, diagnosed with a chronic lower back disease. That same spring, in London, his sister Kathleen married an English nobleman, William Hartington, the heir to the staunchly Protestant Duke of Devonshire. The difference of religion made it a controversial match from both families' perspectives–Rose Kennedy even went into seclusion for a while, claiming that she had "lost" a daughter. But Kathleen had the support of her brother Joe, who was then in London flying missions against German submarines, and so the marriage went forward.

By this point, Joe Kennedy, Jr. had been flying missions against the Nazis for some time, even turning down a chance to return to the U.S. in order to keep flying. Later, some would claim that JFK's sudden celebrity from the PT 109 incident rankled his older brother, and drove him toward a reckless pursuit of heroism. In any case, what became Joe Jr.'s final mission was an almost suicidally dangerous operation that consisted of dropping ten tons of high-explosive TNT on a German target in France. The mission proved fatal, as Joe Jr.'s plane exploded in the air over southern England on the evening of August 12, 1944. The devastating news reached the Kennedy family's summer home, in Hyannis, Massachusetts, a day later. The family was united in grief, and their sorrows only increased in September, with the news that Kathleen's husband had been killed in the war.

While JFK, now the eldest Kennedy son, worked to put together a memorial book for Joe Jr., Joe Sr. became consumed by bitterness. As World War II, in which he had opposed U.S. involvement, wound to a victorious conclusion, Joe Sr. threatened to take out his frustrations on Franklin Delano Roosevelt and the Democratic Party. He had to be talked out of endorsing Roosevelt's Republican opponent in the 1944 election, Thomas Dewey, and in a private interview, accused the president of filling his cabinet with "Jews and Communists." As his father's anger mounted, JFK's back trouble continued unabated, and the hero of PT 109 received a medical discharge from the navy on March 1, 1945. Returning to his family, JFK soon found himself the focus of his father's thwarted ambitions. Joseph Kennedy, Sr. had seen his eldest son die in a war that he himself had opposed, and he now channeled all of his energies and ambitions into a political career for his second-born son. "It was like being drafted," JFK later described it. "My father wanted his oldest son in politics. 'Wanted' isn't the right word. He demanded it." In JFK, the Joe Sr. found a willing vehicle for his ambition.

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