Why does in god we trust not violate the constitution?

[Major Nikon]

31. They had all sorts of problems with state religions

People like Jefferson and numerous others spoke about the dangers of entanglements with religion and state. I know by "state" you mean individual states formed the union, but it's really the same thing especially in respect to how the founding fathers viewed the subject. The Bill of Rights didn't even apply to the states for almost another hundred years so your idea of them doing nothing about the state question implies apathy on the subject doesn't make much sense from a historical perspective.

As far as allowing prayer in opening congressional sessions go, this was protested from the very beginning and has never been without controversy or challenge. The SCOTUS ultimately ruled the framers viewed it as a toleration of the religious views of the membership and not an official sponsorship.

The OP is not suggesting our government should be anti-religious. Only that there should be a line between toleration and entanglement which shouldn't be crossed. This is an idea that was well established from the very beginning.