The theatre company began after businessman and philanthropist Leo M. Bernstein purchased the property, along with the nearby Wayside Inn and other buildings in the surrounding area.

After years of lower ticket sales, a reduction in grants and other funding, and the expenses of a needed renovation that was completed in 2008, Wayside board members closed the theatre in August 2013.

[3] On February 22, 1962, Dwyer sold the property to Leo M. Bernstein, a real estate developer, banker, and philanthropist from Washington, D.C.[3][6] Bernstein had previously purchased and restored the nearby Wayside Inn, a historic building and the namesake of Wayside Theatre which opened as a tavern in 1797, and restored numerous other properties in the area including the Hotel Strasburg, Stonewall Jackson Museum, and Crystal Caverns in Strasburg, the Battletown Inn in Berryville, and the Burwell-Morgan Mill in Millwood.

[16] After Come Blow Your Horn, plays performed during the 1963 season included Charley's Aunt, Summer and Smoke starring Peter Boyle and Lowry, Bus Stop, Light Up the Sky, The Fantasticks, The Drunkard, Misalliance, and Two for the Seesaw.

Echoing the plans made by Bernstein, he advertised the theatre as a place to visit during the busy tourist season, which runs from May through autumn in the area surrounding Skyline Drive.

[23][25] A bus tour company from Washington, D.C., offered a weekend excursion package that included a stay at the Wayside Inn, a ticket to the theatre, and meals, along with visits to Harpers Ferry, West Virginia, all for $33.25 per person.

Slavet's group ensemble, The Garrick Players, were among the actors during his first year after the five members had been evicted from their space at Grace Episcopal Church in Washington, D.C.[34][35] The 1968 season was postponed due to the assassination of Senator Robert F. Kennedy and the national observance that followed.

[46][47] That year Wayside celebrated its 10-year anniversary, based on the premise the Maralarrick Players had performed in 1962, which was the subject of many news articles praising the theatre and noting its importance to the local cultural scene.

[55] Furman received additional criticism for his handling of the company during the first half of his second year, with local media continuing to notice faults in play selection and technical details.

[69] Actors who performed at Wayside in the 1970s, in addition to the aforementioned group from Story Book Theatre, include Cara Duff-MacCormick, whose mother accepted her Theatre World Award while her daughter was performing at Wayside, future Tony Award-winner Donna McKechnie, Richard Bauer, Ken Olfson, and Tandy Cronyn, daughter of Jessica Tandy and Hume Cronyn.

[75][76] Some of the plays performed at Wayside during that decade include A Funny Thing Happened on the Way to the Forum, You're a Good Man, Charlie Brown, Irma La Douce, Cat on a Hot Tin Roof, Once Upon a Mattress, and Hamlet.

[77] It was revealed under Kirkman, the deficit had grown from $10,000 to more than $80,000, partly because of an unsuccessful venture of planned William Shakespeare performances that proved unpopular and cost $30,000 to produce.

It was also decided in order to cut expenses, the season would only include three plays, each performed by only two actors with minimal set designs, in addition to the annual Christmas show.

[98] The performances that season received praise from critics, especially Driving Miss Daisy, but it was noted in reviews from Romance/Romance, that due to sexual innuendos used in the script, "many ticketholders not only didn’t return for the second act but some left after it began.

[105] Amadeus was lauded by critics and is noted as being "perhaps one of the most expensive in Wayside’s history and perhaps one of the most beautiful" due to the cast of 19 actors, the almost three dozen period costumes and wigs that were used, an elaborate stage design, and music.

[108] An article in The Winchester Star noted "For the first time, the second-oldest theatre company in the state, will stage the first regional production of a major Broadway hit.

[125] During this time period, there were hopes of the theatre company moving to a new cultural center that Lord Fairfax Community College was raising funds to build.

"[88] During his first year as artistic director, Warner Crocker hired actors not only from New York City, Washington, D.C., and the local area, but also from Chicago, where he had previously worked.

"[128] In addition to Jackson, actors who appeared at Wayside in the 1990s include Sam Gold, who would later become a Tony Award-winning director, Clark Middleton, David Engel, Ron Palillo, and Bart Shatto.

[111][130][131][132][133][134] Plays performed at Wayside that decade include A Walk in the Woods, The Lion in Winter, I Hate Hamlet, Equus, Marvin's Room, The Mousetrap, and La Bête.

Around that same time Wayside began to host stage readings by theatre staff and locals that took place on weekends from January to April, a new venture that was repeated the following two years.

Changes to the theatre included enlarging the stage by expanding the back portion of the building, renovating the bathrooms, new lighting, new plumbing, new seats, and new roof support beams.

One way management reduced expenses was by replacing the staging of Lies and Legends, the Songs and Stories of Harry Chapin, which would have involved paying a large sum in royalties, with Southern Crossroads, created by Crocker and Steve Przybylski.

[167] Plays performed at Wayside during the 2000s include All I Really Need to Know I Learned in Kindergarten, Laughter on the 23rd Floor, The Spitfire Grill (musical), Othello, and Man of La Mancha.

[168] In 2010 theatre officials held public meetings to inform locals of the financial issues and a fundraising event at Lord Fairfax Community College took place.

Money-saving measures followed including firing two staff members and, similar to Wayside's 1980s financial crisis, the theatre ended its affiliation with the Actors' Equity Association.

[170] The success of Wayside's annual Christmas play and a well-attended staging of Greater Tuna in 2012 did help alleviate some financial stress, but the theatre's debt remained high.

[174] Despite the announcement of Wayside's potential closure, one reporter noted after seeing Smoke on the Mountain: Homecoming: "no one could tell a dark cloud looms over the theater on Main Street of Middletown with the excellent acting and musical performance of the cast.

[176] By March he announced Wayside had raised almost $86,000 and, not only would the theatre remain open, plans were being made for the 2013/2014 season and fundraising events would take place that June and December.

[179] Boeing-Boeing was intended to run until August 11, but during rehearsals of the next planned production, I Love You, You're Perfect, Now Change, board members announced Wayside was $1 million in debt and would close effective immediately.