After the 1956 election, many commentators began to speculate about the possibility of JFK making a run for the White House. He did nothing to dampen this buzz, and began laying the groundwork for a presidential bid by accepting frequent speaking engagements around the country. Nor did it hurt that his book, Profiles in Courage, was awarded the prestigious Pulitzer Prize for biography in 1957. That JFK's well-written, but hardly spectacular, work captured the Pulitzer was a surprise, and many have attributed his receipt of the award to the behind-the-scenes machinations of his father's associates. Regardless, winning the Pulitzer gave the handsome, popular senator yet another upward boost, and no one outside the Kennedy inner circle knew that JFK had not actually written it.

In the Senate, meanwhile, JFK walked a tightrope between the Democratic Party's competing interest groups–the liberal wing, which loved Adlai Stevenson but mistrusted the less ideological JFK, and the southern wing, which was conservative and bitterly opposed to the ongoing Civil Rights Movement. In 1957, JFK was given membership on the powerful Senate Committee on Foreign Relations. There, he muted the strident anti-Communism he had displayed during the McCarthy era, in favor of an emphasis on economic aid to the Third World. Additionally, he denounced France's ongoing effort to hold onto its colony in Algeria, a stance that endeared him to liberals. On civil rights issues, meanwhile, JFK tried to placate Southern Democrats by hewing to a middle ground, supporting some civil rights measures while opposing others. This was a pragmatic plan of action, perhaps, since JFK needed to broaden his base of support beyond Catholics and northeasterners. Many blacks, however, came to regard him with suspicion, as a result of this unwillingness to commit to a full civil rights agenda.

After a tragic miscarriage following the 1956 convention, meanwhile, Jackie Kennedy gave birth to her first child, Caroline Bouvier Kennedy, on November 27, 1957. The Kennedy marriage was difficult–JFK was frequently away from home for long stretches (he was vacationing in Europe while Jackie endured her miscarriage), and his penchant for womanizing had continued even after their wedding. It was an era in which the press kept matters of sexual indiscretion tightly under wraps, and the public never knew about JFK's multiple affairs, which only increased as his fame and prestige grew. But Jackie almost certainly knew, and it placed a strain on her union with her husband.

In November 1958, JFK won reelection to the Senate by a huge margin, capturing seventy percent of the vote. Buoyed by this victory and by his increasing visibility, he became a clear front-runner for the Democratic nomination in 1960. Still, the issue of his Catholicism stirred controversy in late 1950s America, and JFK made a number of speeches in which he asserted that his faith would have no impact on his handling of the presidency–that he would make sure that church and state remained safely separate. His promises, and the growing tolerance of religion in America, had their effect, and he swept through the Democratic primaries in 1960, handily defeating his principle adversary, Minnesota Senator Hubert H. Humphrey, Jr. In that era, however, a victory in the primaries did not guarantee a candidate the nomination, and JFK needed every ounce of political muscle to defeat the still-popular Stevenson and Senate Majority Leader Lyndon Baines Johnson at the Democratic Convention. Having won the nomination, JFK made an unlikely but crucial alliance–he tapped the conservative southerner Johnson as his running mate. America was on the edge of a "New Frontier," JFK told the convention, a phrase that was to resonate throughout the campaign.

The Cold War was a dominant issue during the campaign for the presidency. JFK accused the Republicans of having allowed a "missile gap" to grow between the United States and the U.S.S.R., warning that the Soviets had pulled ahead in the nuclear arms race. Feeding his argument was the fact that with their launch of Sputnik in 1957, the Russians had sent a satellite into orbit long before the Americans managed to do so (the U.S. launched its first satellite, Explorer-I, in 1958). The launch of Sputnik had instilled in many people a fear that the United States was losing the struggle against Communism, and JFK played on those fears. Still, the election was remarkably tight–one of the closest in U.S. history–and little details helped decide the matter. During the presidential debate–the first ever televised– JFK appeared virile and commanding, whereas Nixon looked haggard and unshaven. Also critical was JFK's sympathetic phone call to the wife of Martin Luther King, Jr., the civil rights leader, while King was in jail for civil disobedience. The symbolism of the phone call was crucial in helping improve JFK's image in the black community.

In the end, JFK and Johnson won by fewer than a hundred thousand votes. They captured 303 electoral votes to 219 for Nixon, with the difference coming in the populous states of Illinois and Texas (Johnson's home state), where there were widespread allegations of voter fraud on behalf of the Democratic team. But the results were ultimately ratified, and John F. Kennedy officially became the President-elect of the United States. A few weeks after the election, more good news came with the birth of his son, John F. Kennedy, Jr.

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