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The Fifteenth Street Presbyterian Church was founded in 1841 as the First Colored Presbyterian Church by educator and pastor John F. Cook, Sr. (ca. 1810-1855). Its first home was Cook's small frame schoolhouse, Union Seminary (formerly the Smothers School) at 14th and H streets, NW. The first church building was erected on 15th Street between I and K streets in 1853. The church moved to 15th and R streets in 1918. The current building was completed in 1979.

John F. Cook, Sr., the first black Presbyterian pastor in the city, was born enslaved. His aunt, Alethia Browning Tanner, purchased his freedom, in addition to that of other family members, with money raised from vegetables she marketed at Lafayette Square. In 1834 he became schoolmaster of Union Seminary, where he would establish the church and serve as its first pastor. A year later, Cook temporarily fled the city during the Snow Riot, when a white mob attacked and burned down the one-room schoolhouse.

Rev. Henry Highland Garnet, an ardent abolitionist and orator, served as pastor of the Fifteenth Street Presbyterian Church from 1864 until 1866. When Congress passed the 13th Amendment officially ending slavery in the United States, Garnet was invited to preach a sermon before the House of Representatives. Rev. Francis J. Grimke (1850-1937) served the church as pastor for more than 50 years, beginning in 1877. He used his pulpit to call for civil rights, campaigned against racism in American churches, helped found the American Negro Academy in 1897, and worked toward the creation of the NAACP.

The church has been a vital religious, educational, and social center. It was the first home of the Preparatory School for Colored Youth, the city's first public high school and the first black high school in the United States. Sojourner Truth held benefits for the Colored Soldiers' Aid Society at the church. Seamstress and memoirist Elizabeth Keckley organized church members in an emancipation celebration in April 1863 to commemorate the first anniversary of the DC Emancipation Act.

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