In his celebrated speech to the Greater Houston Ministerial Association on September 12, 1960, Democratic presidential candidate John F. Kennedy declared unequivocally that he believed "in an America where the separation of church and state is absolute - where no Catholic prelate would tell the President (should he be Catholic) how to act, and no Protestant minister would tell his parishioners for whom to vote - where no church or church school is granted any public funds or political preference - and where no man is denied public office merely because his religion differs from the President who might appoint him or the people who might elect him." Kennedy went on to make it clear that he regarded the Jeffersonian wall of separation not as a flexible metaphor but as the foundation of the American system of government. He reminded his audience, composed heavily of evangelical Protestants, that Jefferson's religious freedom act in Virginia was strongly supported by Baptists who had endured persecution both in England and in America. With a nod to the non-religious, the candidate also expounded his vision of American as a nation "where every man has the same right to attend or not attend the church of his choice." Kennedy's speech was widely regarded as one of the turning points of his campaign; he was addressing the fears not only of southern evangelicals, who in 1928 had rejected Al Smith because of his Catholicism, but of mainstream Protestants and Jews, who also had serious reservations about a Catholic in the White House. Norman Vincent Peale, the best-known Protestant cleric to voice his doubts, had flown in from New York for Kennedy's speech and press conference.

…today [JFK's] forthright support for a "wall of separation" would antagonize not only the evangelicals he won over in 1960 but the hierarchy of his own church. Kennedy's belief in an America where "no church or church school" would be eligible for tax support has been rejected by nearly all Republicans and a fair number of Democrats, fearful of being left behind as the faith-based bandwagon rolls on. As for the Catholic Church, the authoritarian Pope John Paul II …created problems for American Catholic politicians who thought that "dual loyalty" issues had been laid to rest in Kennedy's generation. In January 2003, the Vatican issued an innocuously titled "Doctrinal Note on Some Questions regarding the Participation of Catholics in Political Life," but the bland packaging was misleading. The "doctrinal note" was an order to Catholic officeholders to toe the line on abortion, physician-assisted suicide, and gay marriage - even if official church teaching conflicted with the politician's personal conscience and sense of public duty. (Senator Edward M. Kennedy, commenting on the Vatican effort to turn back the clock for American Catholic politicians, referred to his brother's Houston declaration that "I do not speak for my church on public matters - and the church does not speak for me.")

"…no man shall be compelled to frequent or support any religious worship, place, or ministry whatsoever, nor shall be enforced, restrained, molested, or burdened in his body or goods, nor shall otherwise suffer on account of his religious opinions or belief; but that all men shall be free to profess, and by argument to maintain, their opinions in matters of religion, and that the same shall in nowise diminish, enlarge, or affect their civil capacities."

The Virginia Act for Establishing Religious Freedom, Thomas Jefferson, 1786