A directive sent by Republican state Superintendent Ryan Walters said the rule was compulsory, requiring immediate and strict compliance.
The rule will apply to lessons for all public school students aged from around 11-18.
It comes a week after Louisiana’s governor signed a law directing all public schools in that state to display the Ten Commandments.
In a statement, Walters described the Bible as “an indispensable historical and cultural touchstone.
His announcement, which covers grades five to 12, drew criticism from civil rights organisations and groups that advocate for a strict separation of church and state.
Walters has previously argued that secularists in the US have created a state religion out of atheism, by driving faith away from the public square.
In an op-ed last year for Fox News, he wrote that US President Joe Biden and the teacher unions had supplanted biblical values with “woke, anti-education values that tell students that they should treat their classmates differently depending on their race and sex and that they should be taught graphic sexual content at a young of an age as possible.
In a statement, the Interfaith Alliance – a US group that seeks to protect religious freedoms – called the Oklahoma superintendent’s directive blatant religious coercion.
It comes a week after Louisiana ordered all classrooms up to university level in the state to display a poster of the Ten Commandments.
Days later, nine families in the state sued Louisiana, marking the start of what some expect will be a protracted legal battle.
The complaint, backed by civil rights groups, argues that such a display violates the First Amendment of the US Constitution, which guarantees freedom of religion, and that the display “pressures” students into adopting the state’s favoured religion.
There have previously been legal battles over the display of the Ten Commandments in public buildings, including in courts, police stations and schools.