The church grew and prospered until 1838, when the "New School-Old School Controversy", a dispute regarding slavery, caused 72 of its 187 members to leave and form, as New School adherents, The Third Street Presbyterian Church. The pastor who preached at Abraham Lincoln's funeral, The Rev. Phineas Gurley, served First Church from 1849 to 1854.

For 81 years the two churches, only a city block apart, maintained their separate congregations. However, in 1919, their differences long forgotten, the two churches were reunited to become a congregation of 1146 members. They had a vision of creating more than just a church. They also launched a Choir College. They chose the name Westminster, both for the church and the Choir College.

This reunited congregation worshiped in Dayton's Memorial Hall until the current building was completed in 1926. Architect Ralph Adams Cram designed this neo-gothic structure, keeping two things in mind: the building was to house the Westminster Choir College and the Te Deum Window from the First Presbyterian Church, a creation of Tiffany Studios. The Choir College has since outgrown our church and is currently housed in Princeton, New Jersey, and is part of Rider College.

From September of 1999 through May of 2000, Westminster celebrated the 200th birthday of Dayton's first church.