Originally 21.5 acres (87,000 m2) on the estate of James M. Ware, it was already a burial ground by April 1869 when it served as the resting place for the infant daughter of future mayor Robert H. Henley.

Most of the 10,000 or so burials at Oak Hill were interred before 1930, including nine of the ten landholders who founded the city, many early mayors, a Revolutionary soldier, numerous American Civil War veterans, and the first male child born in the city.

Although few records exist from the time, most believe the "Potter's Field" section was also used as the final resting place for many victims of the 1873 cholera epidemic.

In 1928 the caretaker's cottage near the center of the property, was removed to the southwest corner of the cemetery and a new "Pioneer's Memorial Building" was constructed of Indiana limestone, designed by Miller & Martin architects with William Kessler, landscape architect.

Media related to Oak Hill Cemetery (Birmingham, Alabama) at Wikimedia Commons