This cemetery is the largest in the Ingersoll area. It officially opened in August 1864. The first grave was dug in the center of the cemetery on the highest point of the hill in what is now Section H. Jane Williams was buried there on August 19th 1864. She was single, age 31, and died of diphtheria. In subsequent years the cemetery was not only used for new burials, but the graves from many small graveyards and backyard grave sites were transferred here. To date there are over 12,000 burials in the cemetery. It includes a mausoleum, 3 columbariums and 24 sections. One section which is being preserved is the historic Potter's Field, though it is no longer being used.

Land consisting of 17 acres situated in North Oxford and adjoining Ingersoll was purchased for a cemetery in 1864 by a group of 168 local residents who became shareholders in the Ingersoll Rural Cemetery Company. The first meeting was held May 21, 1864, and the board elected: president, D. M. Robertson; treasurer, Charles E. Chadwick; W. A. Ramsey, Donald Wallace, Adam Oliver, James Noxon, Warren Harris, James Wallace, and William McDowell. J. W. Canfield was appointed secretary, and G. W. Wonham was the surveyor.

There was a diphtheria epidemic at the time. Of the first 25 buried, 14 were children, and 11 of those died of diphtheria. In 1882, the committee decided no more interest was to be paid to the shareholders. In 1927, a mausoleum was erected. The cemetery became a municipal cemetery on August 1, 1955.

The Potter's Field is located at the back of the cemetery. Approximately 400 people are buried there without individual headstones, including individuals who experienced poverty, children, former slaves, Chinese immigrants, and other marginalized residents. In June 2025, a monument was unveiled listing the names of those interred, recognizing them as members of the community. The identities were determined through burial records by Western University students and researchers, with support from the Town of Ingersoll and Zorra Township, and in some cases ground-penetrating radar was used to help confirm burial locations.