The Klezmatics came together in New York's East Village in 1986, out of a classified advertisement clarinetist Rob Chavez placed in the Village Voice looking for anyone interested in playing klezmer. Trumpeter Frank London, then a recent New England Conservatory graduate who had been learning the Hasidic wedding repertoire on the job, answered it and brought in singer and accordionist Lorin Sklamberg. The inaugural lineup added violinist Alicia Svigals, clarinetist Margot Leverett, drummer David Licht, and bassist David Lindsay; Paul Morrissett, a Colorado-born folk multi-instrumentalist who had come to the music through international folk dancing, replaced Lindsay on bass and tsimbl before the band's first record. The name was a joke on the punk group the Plasmatics, and the joke was load-bearing: this was a klezmer band assembled by downtown musicians who had no interest in treating Yiddish music as a preservation project.

The band's first records were made for the Berlin label Piranha. Shvaygn = Toyt, released in 1989 (the band's own site dates it 1988), took its title from the ACT UP slogan "Silence = Death" rendered in Yiddish, an opening statement of political intent from a group that was, from the start, openly queer and openly activist. Rhythm + Jews followed, recorded and mixed at Lunapark Studio in Berlin in December 1990 and released in 1991, with David Krakauer on clarinet and bass clarinet; The Rough Guide to World Music later called it one of the greatest klezmer records ever made. Jews With Horns, cut at Baby Monster Studios in New York in June 1994, widened the audience further, and four of its tracks began life as commissions for Gregg Bordowitz's 1993 AIDS documentary Fast Trip, Long Drop. Matt Darriau, a New England Conservatory Third Stream graduate who leads the Balkan-jazz group Paradox Trio, joined during the mid-1990s and has held the reed chair since.

The second half of the 1990s put the band in front of audiences well outside the klezmer world. Violinist Itzhak Perlman recruited them, along with Brave Old World, the Andy Statman Klezmer Orchestra, and the Klezmer Conservatory Band, for In the Fiddler's House, recorded in New York on August 6 to 9, 1995 for EMI Classics, with a Radio City Music Hall concert on July 2, 1996 issued as Live In The Fiddler's House and a PBS Great Performances broadcast to follow. In parallel the group wrote the score for Tony Kushner's stage adaptation A Dybbuk: Between Two Worlds, excerpts of which fill the back half of Possessed (1997, Piranha/EFA), an album that also brought in organist John Medeski and carried liner notes by Kushner himself. In 1998 the band recorded The Well (Di Krenitse) with the Israeli singer Chava Alberstein for Xenophile Records, setting fifteen Yiddish poems to Alberstein's melodies in Klezmatics arrangements, produced by Ben Mink. It was named one of the ten best pop albums of 1998 by LA Weekly and, per the band's own account, won a 1998 GLAMA award.

The lineup changed at the turn of the century. Svigals, a founding member and the band's violinist for roughly seventeen years, left in 2002; the Forward subsequently reported that the group settled a sex-discrimination claim she brought over her dismissal. Lisa Gutkin, whose background ran through Irish, bluegrass, and classical playing, took the violin chair and first appears on Rise Up! = Shteyt Oyf! (Rounder, 2002), whose basic tracks were laid down at RPM Sound in New York in February 2002 and which includes four pieces from the band's score for Pilobolus Dance Theatre's Davenen. Two years later came the first live album, Brother Moses Smote The Water, recorded July 31, 2004 at the Berliner Heimatklänge festival with the Hebrew gospel singer Joshua Nelson and vocalist Kathryn Farmer, a klezmer-and-gospel meeting that has stayed in the band's repertoire ever since.

The widest audience arrived through Woody Guthrie. Nora Guthrie and the Woody Guthrie Foundation invited the band to set previously unpublished lyrics from her father's archive to new music, and the resulting Wonder Wheel (Jewish Music Group, 2006), recorded across Loho Studios in Manhattan, GoodandEvil in Brooklyn, Stoney Clove Studio in Chichester, New York, and Darriau's house, won the Grammy Award for Best Contemporary World Music Album at the 49th Grammy Awards in 2007, making the Klezmatics the only klezmer band to win one. A companion record of Guthrie's Hanukkah lyrics, Woody Guthrie's Happy Joyous Hanukkah, followed on September 5, 2006. Around the same time the drum chair turned over: Richie Barshay, a jazz percussionist then working in Herbie Hancock's quartet, was recruited in October 2005 to replace David Licht, who stepped back to focus on family. The band's twentieth-anniversary concert at New York's Town Hall on March 5, 2006 was filmed for Erik Greenberg Anjou's documentary The Klezmatics: On Holy Ground and issued on record in 2011 as Live At Town Hall.

Four decades in, the band still records. Piranha's Tuml = Lebn: The Best Of The First 20 Years (2008) collected the early catalog; Apikorsim / Heretics (World Village, 2016), produced by Danny Blume, was the first Klezmatics album made with no outside guests or session players at all. Letters to Afar (Chant Records, 2021) is their furthest move from the dance floor: a score for Péter Forgács's installation built from 1920s and 1930s home movies shot by New York Jewish immigrants visiting Poland, drawn from the YIVO Institute archive where Sklamberg works as sound archivist. Piranha reissued the 1990 Berlin sessions as Rhythm + Jews Revisited on vinyl on October 24, 2025, with alternate takes and mixes remastered at Traumton Studios. We Were Made For These Times, released March 14, 2026 on Asphalt Tango Records with Joshua Nelson and the Lavender Light Gospel Choir, marks the band's fortieth anniversary.

The Klezmatics are a klezmer band, not a jazz band, but the distinction has been porous since their first rehearsal: the group's method is to treat Yiddish dance tunes, nigunim, and Yiddish poetry as living material to be improvised on and rearranged, which is a jazz musician's relationship to repertoire applied to a different songbook. That footing is personal rather than theoretical. Frank London took a degree in Afro-American music at the New England Conservatory in 1980 and has spent decades in John Zorn's Radical Jewish Culture orbit on Tzadik; Matt Darriau came through the same school's Third Stream program in the early 1980s and was named by Jazziz among the musicians who did most to bring Balkan and world rhythms into jazz; Richie Barshay arrived from Herbie Hancock's quartet, with recording and touring credits alongside Chick Corea, Esperanza Spalding, Fred Hersch, Kenny Werner, and Lee Konitz. The sound that results is loud, brass-forward, rhythmically layered, and unafraid of ostinato vamps that leave room for a soloist, with Sklamberg's high, unforced tenor carrying Yiddish texts that are as likely to be a queer AIDS-era protest lyric or a Woody Guthrie manuscript as a wedding tune. Critics have consistently treated them as the defining band of the klezmer revival rather than one of its curators, and the band has made the same point in its own terms by scoring Kushner, Pilobolus, and Forgács as readily as it plays freylekhs.