The Constitution of the United States requires the Federal Government and state governments not to infringe the rights of U.S. citizens to believe in whatever religion they choose, if any. The First Amendment has been binding on the Federal Government since the Bill of Rights was ratified by three-fourths of the states in 1791, while it has been binding on the states since the Fourteenth Amendment was adopted in 1868.
However, the Constitution does not mandate tolerance or acceptance of the religious beliefs and practices of others on the level of social discourse.
Although this is probably obvious to most people, it is still worth pointing out that discursive tolerance is not the virtue enshrined in the First Amendment, nor is the separation of religion and public life.
The framers of the Constitution were fully aware that the majority of Americans were deeply religious people, and would neither keep religion out of public life nor extend intellectual acceptance to religions they consider fundamentally incorrect.
The only tolerance envisioned by the framers of the Constitution was tolerance in the sense of freedom from physical persecution for one's religious convictions. Tolerance in this sense is required of all levels of government and all private citizens, even though private citizens may of course vocalize disapproval of the religious choices of others.
Above all, even if people believe that intellectual tolerance and acceptance of the religious beliefs of others is virtuous, the Constitution does not now nor did it ever encourage (or discourage) this belief.