The extreme hostility towards atheists in America can probably be traced to two related factors: America's view of itself as a religious nation entrusted with a special mission from God and America's fight against communism in the Cold War. These two combined to portray atheists as a godless enemy, a fifth column either for Satan or for totalitarian communism.
In The Atheist: Madalyn Murray O'Hair, Bryan F. Le Beau writes:
To understand why atheists met with persistent, ardent opposition, it is important to recall that for most of their history Americans considered the United States Gods New Israel a redeemer nation. This view was especially pronounced during the Cold War, when Madalyn Murray brought her case against school prayer to the Supreme Court. But it was an idea born at the very settling of the British colonies of North America, encapsulated in the rhetoric of Puritan John Winthrop in his shipboard sermon, A Model of Christian Charity.
Winthrop sowed the seeds of Americans thinking of themselves as a nation set apart from the rest of the world by employing language of the Hebrew Bible. They had entered into a covenant with God, he explained, whereby in exchange for his blessing and protection, they would undertake an errand into the wilderness to become like a city on a hill, providing a model of Christian charity for the world. They could fail only if they failed to honor their covenant with God. [...]
The notion of America as a City on the Hill comes with a lot of drawbacks. Such framing causes America to stop being just a nation and to become, in addition, a religion. This attitude is so deeply ingrained in America that most people are completely unaware of it especially more secular-minded Americans who believe they have rid themselves of many traditional religious beliefs.
This passionately held, religious faith in American exceptionalism and the American duty to bring the Light to the rest of the world leads to a messianic fervor that encourages chauvinistic, aggressive contempt for those who fail to believe with the same fervor. People who disagree with Americas policies or actions dont simply have a political dispute with America; instead, they become heretics who must be shamed or eliminated.
Although the Cold War reshaped, even distorted, many aspects of American life, there was little fundamentally new about American Culture in the Cold War era. Most of the characteristics by which we define it were the result of long-standing concepts... The principal effect was psychological. During the 1950s, Americas belief in itself as a redeemer nation took on millennial overtones. In large part due to the threat of nuclear war, many believed that an apocalyptic confrontation between Gods chosen nation and the forces of godless communism would usher in the millennium, the thousand-year earthly reign of Christ as foretold in the Book of Revelation.
This added to the urgency of the battle against atheism and Madalyn Murray OHair, As one observer pointed out, whenever their opponents began railing against those atheists, the latter ceased to be individuals who mattered to God. Instead, they become a monolithic mass of faceless enemies and in a war, theres no fraternizing with the other side
Its interesting that during the earliest years of the Cold War, there was little in the way of religious arguments against communism. Communists may have been an enemy, but the fact that they were a godless enemy didnt seem to matter a great deal. By the early 1950s, though, religious and political leaders realized that religious opposition to communism could be a strong motivator, even stronger than political opposition might be.
This is not to say that they were disingenuous in mounting religious arguments against communism, but it suggests that these religious arguments were not necessary for opposition to communism. Transforming anti-communism into anti-godlessness, though, required turning America even more against atheists, agnostics, liberal religious believers, and skeptics of various sorts. Religious doubters and skeptics were transformed into not just an enemy of religious institutions, but of political institutions as well a Cold War legacy which continues to affect American politics today.