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Nixon almost never got his chance to be on the Republican ticket that year. The media reported that Nixon had a political fund, maintained by his backers, which reimbursed him for political expenses. While not illegal, this accusation exposed Nixon to allegations of possible conflict of interest. Pressure mounted for Eisenhower to dump Nixon from the ticket. Nixon came up with a clever damage control scheme. He went on television to deliver an address to the nation on September 23, 1952, which became known as the Checkers speech, (a reference to a dog named Checkers that the Nixons had received as a gift.) The address was heard by about 60 million Americans, the largest television audience up to that point. Nixon emotionally defended himself, stating that the fund was not secret, nor had donors received special favors. He described himself as a man of modest means. He said that his wife did not have a mink coat. She wore a "respectable Republican cloth coat". He said that there was one gift that he had received, but which he would not give back: "a little cocker spaniel dog sent all the way from Texas. And our little girl—Tricia, the 6-year-old—named it Checkers." The speech resulted in a huge public outpouring of support for Nixon, and Eisenhower was left with no choice but to keep Nixon on the ticket, though some have speculated that this planted the seeds of resentment by the president towards his running mate
Eisenhower gave Nixon responsibilities during his term as vice president—more than any previous vice president. Nixon attended Cabinet and National Security Council meetings and chaired them when Eisenhower was absent. He went on a 1953 tour of the Far East, and later to South America, the latter at personal risk when a mob of protesters attacked the car that Nixon was riding in.
Despite intense campaigning by Nixon, Republicans lost control of both houses of Congress in the 1954 elections. Nixon took these losses personally and considered leaving politics once he had served out his term. But on September 24, 1955, President Eisenhower suffered a heart attack. At first his condition was believed to be life-threatening. Eisenhower was unable to perform his duties for six weeks. The 25th Amendment to the United States Constitution had not yet been proposed. Although Nixon had no formal power to act, he stood in for the President, presiding over Cabinet meetings and making sure that there were no power struggles in Cabinet.
His spirits buoyed, Nixon sought a second term, despite the fact that some of Eisenhower's aides aimed to displace him. In a December 1955 meeting, Eisenhower proposed that Nixon not run for reelection in order to give him administrative experience before a 1960 presidential run and instead become a member of Eisenhower's Cabinet. Nixon believed such an action would destroy his political career. When Eisenhower announced his reelection bid in February 1956, he was coy on the question of whether Nixon would be his running mate. Although no Republican was opposing Eisenhower, Nixon received a substantial number of write-in votes against the President in the 1956 New Hampshire primary election. In late April, the President announced that Nixon would again be his running mate and the ticket was reelected by a comfortable margin in the November 1956 election.
In early 1957, Nixon undertook another major foreign trip, this time to Africa. On his return, he helped guide the Civil Rights Act of 1957 through Congress. The bill was a weakened one and civil rights leaders were divided over whether Eisenhower should sign it. Nixon advised the President to sign the bill. Eisenhower suffered a mild stroke in November 1957, and Nixon gave a press conference, assuring the nation that the Cabinet was functioning well during Eisenhower's absence.
In July 1959 President Eisenhower sent Nixon to the Soviet Union for the opening of the American National Exhibition in Moscow. On July 24, Nixon was touring the exhibits with Soviet Premier Nikita Khrushchev when the two stopped at a model of an American kitchen and engaged in an impromptu exchange about the merits of capitalism versus communism that became known as the "Kitchen Debate".
Nixon was expected to face a serious challenge for the Republican nomination from New York Governor Nelson Rockefeller, the leader of the Republican moderate wing. But Rockefeller announced that he would not be a candidate for president after he completed a national tour which led him to believe that Nixon was too strong of a candidate. After Rockefeller's withdrawal, Nixon faced no significant opposition for the nomination. The Republican Party held primaries in 14 states that year and Nixon won all, except for those in which local "favorite son" candidates (West Virginia and South Dakota) and in New Jersey, which left its delegates unpledged.
At the 1960 Republican National Convention in Chicago, Nixon was the overwhelming choice of the delegates. He received 1,321 votes. His closest rival was conservative Senator Barry Goldwater of Arizona who received only 10 votes. Nixon chose former Massachusetts Senator and United Nations Ambassador Henry Cabot Lodge Jr., as his vice-presidential candidate. It was at this convention Nixon promised to campaign in every state during his campaign.
Nixon's Democratic opponent was his contemporary, Massachusetts Senator John F. Kennedy. The race remained close as Nixon campaigned on his experience, while Kennedy called for new blood and claimed the Eisenhower–Nixon administration had allowed the Soviet Union to overtake the U.S. in ballistic missiles resulting in a "missile gap". The statement was untrue, but in politics, perception is reality. In the campaign a new political medium was introduced in the campaign: televised presidential debates. In the first of four such debates Nixon appeared pale, with a five o'clock shadow, while Kennedy came across as young and refreshed. His campaign was more attuned to how best to present their candidate on black and white television. Although this claim is disputed by others, some of Nixon's biographers have claimed that his performance in the debate was not well-received in the visual medium of television, but that many people listening on the radio thought Nixon was the better speaker.
At the Republican Convention, Nixon had pledged to campaign in all 50 states. In August, Nixon injured his knee on a car door while campaigning in North Carolina. The knee became infected and Nixon had to cease campaigning for two weeks. When he left Walter Reed Hospital, Nixon refused to abandon his pledge to visit every state and he spent time visiting states that he had no chance of winning, or that had few electoral votes. Nixon spent the last weekend before the election campaigning in Alaska, which had only three electoral votes, while Kennedy campaigned in large states such as New Jersey, Ohio, Michigan, and Pennsylvania.
On election day Nixon narrowly lost the election. Kennedy won the popular vote by only 112,827 votes (0.2 percent). There were charges of voter fraud in Texas and Illinois, both states won by Kennedy. Although he was privately bitter as a result of the belief that the election had been stolen from him, Nixon refused to consider contesting the election.