All Souls was founded on March 5, 1911, as a mission church of St. Alban's, Washington, D.C., with the first meeting in a house at 2628 Garfield Street NW.

That fall, the church purchased the lot where it now stands and erected a portable chapel with the first service at the site on October 15, 1911.

In October 1914, the growing congregation consecrated a new permanent home designed in a Tudor gothic revival style with local fieldstone by Frederick A. Kendall, the senior warden at the time. Kendall had worked from 1901-1909 in a partnership with James G. Hill, one of the most famous architects of the day. Together, Hill and Kendall designed several notable buildings in the city, the Ontario Apartments being one.

By 1922, the Vestry had begun raising funds for a larger structure to meet the needs of the expanding congregation. They hired Delos H. Smith to design a larger sanctuary in the same gothic revival style with the same fieldstone. Consecrated in 1924, the new nave ran on an east-west axis and the old nave became the transept. Smith was a locally prominent architect and architectural historian (his papers are at Colonial Williamsburg) whose practice included many churches, among them the rebuilt St. Paul's Episcopal Church Rock Creek in 1922 after it had burned, an addition to All Saints Chevy Chase in 1926, Christ Lutheran Church in 1934 and in 1952 the New York Avenue Presbyterian Church. In addition to his ecclesiastical work, Smith's projects also included local and federal civic commissions such as the 1931 Rockville County Courthouse, and interestingly, the Prayer Room in the United States Capitol.

In 1951, All Souls added its administration wing along Woodley Place, laying the cornerstone in a ceremony with Thomas Clark, a Justice of the Supreme Court. Architect Arthur P. Starr designed this building. Starr had been a draftsman in the offices of Jules H. de Sibour, designer of many of Washington's embassies and office buildings, before he eventually went into private practice with his principal work being a medical office building (since razed) at 1726 I Street along with several local commercial and industrial facilities.

And in 2015, the church completed its accessibility addition with an elevator, two handicapped restrooms, and a sunken garden opening from the undercroft. The site plan, floor plan, and construction supervision and drawings were by MTFA Architecture, but the external design of the building was, again, by a vestryman of All Souls, Frederick Taylor, an architect in private practice in Washington. Taylor ensured that the addition's stylistic elements, gothic revival theme, and meditation garden were all in keeping with the original church design.
