Construction began in summer 1921. Architect Reginald Geare designed the building in collaboration with Harry Crandall, a local theater operator whose chain of D.C. movie houses had become one of the most successful in the country. The Lincoln opened in 1922 as a venue for silent film and vaudeville aimed specifically at Washington's Black community - which segregation barred from most of the city's other major theaters. The exterior was brick, the interior trimmed in Victorian ornament. Behind the proscenium were full backstage facilities for live performance. In 1927, the theater was sold to A.E. Lichtman, who set out to turn it into something even more ambitious: a luxury movie palace with a ballroom attached, the Colonnade, where the city's Black social life could find space the segregated downtown denied it. By 1928, the projector booth was wired for sound, and the Lincoln became one of the first Black-serving theaters in Washington equipped for the talkies.

Through the 1930s and 40s and into the 50s, U Street ran on a current the rest of segregated Washington could not generate. Howard University, two blocks north, fed the neighborhood with students and intellectuals. The U Street Corridor housed Black-owned businesses, Black-owned banks, Black-owned newspapers, Black-owned churches. The Lincoln Theatre and its Colonnade ballroom anchored the entertainment district. Duke Ellington played the Colonnade. So did Cab Calloway, Louis Armstrong, Ella Fitzgerald, Pearl Bailey, and most of the touring jazz and big-band names. In 1952, the Lincoln installed a television projection system - large-screen TV broadcasts shown to ticketed audiences, a peculiar transitional technology of the early television era. The Colonnade was demolished in the late 1950s as the audience habits that had supported it began to fragment.

On April 4, 1968, Martin Luther King Jr. was killed in Memphis. Within hours, U Street was on fire. The riots that followed gutted the corridor - shops burned, businesses fled, residents left. The Lincoln Theatre survived the flames but lost its audience. The neighborhood entered a long decline. In 1978 the building was crudely subdivided into two smaller theaters and renamed the Lincoln Twins. All-night movie programs in the late 1970s drew weekend crowds of a few hundred at a time, but the grand Lincoln of the Ellington years was gone. In 1983, developer Jeffrey Cohen bought the property as part of a $250 million plan for the corridor he called Jackson Plaza. He filed for bankruptcy in 1991. The D.C. government and a local foundation took over the restoration, hired the firm Leo A. Daly to manage it, and reopened the theater on February 4, 1994 - with a performance of Barry Scott's Ain't Got Long to Stay Here, a one-man show about the life of Martin Luther King Jr.

The reopened Lincoln did not have an easy path back. Throughout the 1990s and 2000s the theater required regular financial aid from the D.C. government to stay afloat. Programming was eclectic - the annual LGBT film festival Reel Affirmations ran here from 1998 to 2008. The Black Ensemble Theatre's Jackie Wilson Story played a multi-week run in 2002. The Duke Ellington Jazz Festival launched at the Lincoln in 2005. From 2008 to 2010, Arena Stage used the venue for productions including Carrie Fisher's Wishful Drinking, while Arena's Southwest Waterfront complex was being renovated. Dave Chappelle filmed Killin' Them Softly here for HBO in 2000. By 2011, with city funding cut, the Lincoln faced closure again. The D.C. Commission on the Arts and Humanities took over management and began searching for an operator willing to run the venue commercially.

In June 2013, Mayor Vincent Gray's office announced the new operator: I.M.P., the company behind the 9:30 Club, Washington's most successful independent music venue. I.M.P. began booking the Lincoln that fall, and the room has run nearly continuously since. Janelle Monáe opened with a show on October 14, 2013. Lauryn Hill played February 9, 2014. Sharon Jones and the Dap-Kings ran two nights in February 2014. Experience Hendrix - Bootsy Collins, Eric Johnson, Dweezil Zappa, Buddy Guy - filled the room March 30, 2014. Spoon ran three nights. Nas performed the 20th-anniversary set of Illmatic on October 4, 2014. Kendrick Lamar played November 1, 2015. Patti Smith sat down for a conversation with co-owner Seth Hurwitz on October 12, 2016. Brian Wilson performed Pet Sounds in full for its 50th anniversary on consecutive May 2017 nights. Trevor Noah, Demetri Martin, Hannibal Buress, Louis C.K., and Deon Cole have all filmed comedy specials in the room. The U Street Metro station opened across the street in 1991, completing the corridor's resurrection. Ben's Chili Bowl, next door, has never closed.