It is a Federal-style structure that consists of a two-story, three-bay, gable-roofed central block with a two-part, 1+1⁄2-story saltbox ell on the west side.

The front portion of the ell was built circa 1800 in Hopeton, a settlement two miles east of Dresden which failed early in the nineteenth century.

In 1921 a large committee including Thomas Edison, Luther Burbank, Edgar Lee Masters, and members of the Ingersoll family opened the birthplace as a museum, community house, and public library.

In 1954, a committee led by atheist activist Joseph Lewis restored the building again and operated it as an Ingersoll museum for several years.

[7] Tom Flynn designed the freethought museum at the birthplace of nineteenth century agnostic orator, and was its director from the time it opened to the public in 1993 until his death in 2021.

CODESH Inc., as the Council for Secular Humanism was then known, purchased the property for $7,000 and pressed successfully for its inclusion on the National Register of Historic Places.

Though Flynn was employed at CODESH during this period he was not closely involved with the purchase and rehabilitation, which were orchestrated primarily by chairman Paul Kurtz, then-Free Inquiry editor Tim Madigan, and colleague Richard Seymour.

Grothe on Point of Inquiry, "He [Ingersoll] literally was seen or heard by more Americans than would see or hear any other human being until the advent of motion pictures or radio.

[17] In 2009 the Museum received a large number of artifacts and papers from the estate of Eva Ingersoll Wakefield, Robert Ingeroll's, last surviving granddaughter.

Display cases were refurbished and all-new interpretive signage was developed, including professionally designed mural-sized wall graphics.