Horseback riding has been enjoyed in Rock Creek Park from its beginning. The cost of maintaining or renting horses has limited riding to the more affluent public, for the most part, and many equestrian users of the park have been persons of prominence in local and national affairs. Douglas McKay, President Dwight D. Eisenhower's first secretary of the Interior, and William P. Clark, President Ronald Reagan's second Interior secretary, were regular Rock Creek riders.
Until the 1950s recreational riders were served only by stables outside the park, including Pegasus Stables in Silver Spring, Maryland, and Edgewater Riding Academy near 26th and D streets. In 1956 Helen Fenwick Kollock, manager of Pegasus Stables, and Mary K. Nelms met with Secretary McKay and Superintendent Edward J. Kelly of National Capital Parks to propose a stable in the park. The women would erect it near the existing Park Police stable, built the year before north of Military Road and east of Oregon Avenue, and present it to the government in return for a long-term operating lease. Horses for hire and boarding for individual owners' horses would be offered. 
McKay approved the proposal, but complications soon developed. The Edgewater Riding Academy property was condemned that year for the eastern approach to Theodore Roosevelt Bridge, and its operator, Francis J. Hannan, sought to relocate in Rock Creek and Potomac Parkway. The prospect of two competing private ventures caused the Park Service to decide that it should build the park stable. In March 1957 it announced its intention to do so in fiscal 1958 as a project of MISSION 66, a 10-year development program that would improve facilities throughout the National Park System by the fiftieth anniversary of the Service in 1966. 
Hannan and his patrons formed the Lower Rock Creek Riding Association to lobby for a stable in Rock Creek and Potomac Parkway. At the same time, opposition developed to the site tentatively selected near Oregon Avenue: a stable there would displace garden plots tended by members of the Good Will Garden Club of Chevy Chase. In June Director Wirth, Chief Landscape Architect Robert W. Andrews, and Sen. Francis H. Case of South Dakota inspected the Oregon Avenue site and a site by the William Howard Taft (Connecticut Avenue) Bridge advocated by the Lower Rock Creek Riding Association. They concluded that a stable was needed at each place. 
Notified that their gardening permits would not be renewed in 1958, the Good Will Garden Club members escalated their protest. A delegation including Rep. DeWitt S. Hyde of Maryland, Rep. Peter F. Mack, Jr., of Illinois, and Postmaster Roy M. North of the District of Columbia descended on Superintendent Kelly to complain, and letters followed from Sen. Carl E. Mundt of South Dakota, Sen. Estes Kefauver of Tennessee, Sen. Wayne Morse of Oregon, and Rep. Gracie B. Pfost of Idaho. Neighborhood residents voiced fears of odors, flies, disease, and especially "undesirable elements" forthcoming from a stable. "We believe our sixteen year old daughter will not be safe alone in our home, with the stable help required to care for forty horses, and the people who 'hang around' a stable, nearby," wrote one. The local Hawthorn Citizens Association passed a resolution in opposition, declaring that the stable would be a "definite threat to the long-established property in the area and a hazard to the welfare of the citizens." 
Nor did the Park Police welcome the prospect of a public stable adjoining their facility. Sergeants T. C. Tingle and A. D. Baye warned that it would increase the possibility of disease to their horses, leave them with less corral space, and endanger both their horses and the public by bringing them into close contact. Relaying these views to Superintendent Kelly, Acting Chief Raymond L. Selby concurred and sided with the neighborhood opposition: "The contemplated location is very near to a rather exclusive residential area. Rental stables notoriously attract a 'trashy' class of help and hangers-on, such as will be a continual source of friction with the neighboring residents." 
Yielding to the powerful forces arrayed against the Oregon Avenue site, the Service leadership announced in December a shift of location to a site south of Military Road and east of Glover Drive, where the park maintenance area then stood. In March 1958 the Service awarded a $104,000 contract to Sun Construction Company of Silver Spring, which completed the stable for opening that December. Mary Nelms obtained the concession for its management under the name Rock Creek Stables, Inc. William L. Warfield of Falls Church, Virginia, received an $87,500 contract for construction of the second stable, by the Taft Bridge. It opened in April 1959 under Francis Hannan's management as the Edgewater Riding Academy. Built on the same plan, the two stables each accommodated 40 horses. 
Rock Creek Stables experienced financial difficulties by 1960, and Mrs. Nelms sold her interest the following year. In 1970 its operator was forced to declare bankruptcy as a result of an accident claim. The Edgewater Riding Academy was dislocated in 1970 when the Washington Metropolitan Area Transit Authority occupied its building for Metro subway construction (the Red Line would pass beneath Rock Creek at that point). To replace it, WMATA built a new stable near Rock Creek Stables in 1972 from an award-winning design by the noted Washington architectural firm of Hartman-Cox. Both concessions were then acquired by Rock Creek Park Horse Center, Inc., operated by James H. Warrick, Jr. 
In 1974 Robert Douglas began a program of therapeutic riding for handicapped children at the new stable, known as the Red Barn, with Park Service and other federal grants. The National Center for Therapeutic Riding was formed as a nonprofit charity in 1980 and attracted much favorable notice, aided by a visit from Nancy Reagan after she became first lady. Its quarters proved less successful: the Red Barn suffered from leaking skylights and a deteriorating roof structure to the point of threatened collapse in 1980. The Service condemned the building that July and razed it the following February. The therapeutic riding program moved to the older stable nearby.
Another de-stabilizing event occurred in 1980 when fire destroyed part of the small frame Park Police structure near Oregon Avenue; the stable was replaced two years later. Previously, police horses had acquired additional quarters when WMATA vacated the former Edgewater Riding Academy in 1979 upon completion of Metro construction in the vicinity. The paving of the equestrian trail along Rock Creek and Potomac Parkway for bicycles rendered the area unsuitable for recreational riding, so the police takeover met little or no public resistance.