Situated three blocks from the U.S. Capitol, the museum includes towering bronze gates inscribed with text from the Gutenberg Bible and a soundscape of the 10 plagues, enhanced by smog and a glowing red light to symbolize the Nile turned to blood.
The museum was the brain child of US store chain, Hobby Lobby's owner, Steve Green. Eight years ago he began collecting biblical artifacts that he hoped could become the starting point for a museum.
That vision has been realised with the 430,000-square-foot museum.
Green said the institution he largely funded is meant to educate, not evangelise, though critics are dubious.
Museum administrators have hired a broad group of scholars as advisers.
Lawrence Schiffman, a New York University Jewish studies professor and Dead Sea Scrolls expert, called the museum a "monument" to interfaith cooperation. Exhibits have been planned from the Vatican Museum and the Israel Antiquities Authority.
"There's just a basic need for people to read the book," Green said. "This book has had an impact on our world and we just think people ought to know it and hopefully they'll be inspired to engage with it after they come here."
The building alone has been designed to inspire a sense of wonder.
A 140-foot LED display runs the length of the entrance hall ceiling, bathing the lobby in a changing array of color.
The floors are a mix of shimmering marble from Denmark and Tunisia, complemented by columns of Jerusalem stone.
From two high stories, a glass atrium curves from ceiling to floor, echoing the shape of a scroll and providing a clear view of the Capitol dome and the Washington Monument.
A section dedicated to the Bible's modern-day influence includes a replica of the Liberty Bell, inscribed with a verse from Leviticus, and exhibits touching on slavery, abolition and the civil rights movement.
A motion simulator called Washington Revelations creates the sensation of flying over the nation's capital to see Bi ble inscriptions and references in buildings and monuments throughout the city.
Festivities surrounding the opening include a gala fundraiser for the museum at the Trump International Hotel, a dedication ceremony at the museum with Roman Catholic, Jewish and Protestant religious leaders, and a gala in the museum ballroom.