In 1970, the Juilliard Orchestra took an educational tour to Europe and he was invited to Spoleto the next year as an assistant doing work as a répétiteur, coach and chorus conductor.

[6] Conlon received the conducting award of the American National Orchestral Association, and in 1974 became the youngest conductor engaged for the New York Philharmonic Orchestra's subscription series.

Since his New York Philharmonic debut in 1974 at the invitation of Pierre Boulez, Conlon has appeared with virtually every major North American and European orchestra.

Associated for almost 30 years with the Metropolitan Opera, where he made his debut in 1976, he has conducted more than 250 performances there, leading a wide range of works from the Italian, German, French, Russian and Czech repertoires.

His work there has included a series called "Recovered Voices", a multi-year project during which Conlon presented operas by composers affected by the Third Reich.

[7] In March 2024, Los Angeles Opera announced that Conlon is to conclude his tenure as its music director at the close of the 2025-2026 season, and subsequently to take the title of conductor laureate.

[13] In an effort to raise public consciousness to the significance of works of composers whose lives and compositions were affected by the Holocaust, Conlon has devoted himself to extensive programming of this music in North America and Europe.

[14] This includes the works of such composers as Alexander von Zemlinsky, Viktor Ullmann, Pavel Haas, Kurt Weill, Erich Wolfgang Korngold, Karl Amadeus Hartmann, Erwin Schulhoff, and Ernst Krenek.

In addition to "Recovered Voices" at Los Angeles Opera, each summer when he was music director of the Ravinia Festival, Conlon presented a different composer from this group with the Chicago Symphony Orchestra.

Produced in cooperation with the Juilliard School, it has since been reprised at the Spoleto Festival in Italy, the Ravinia Festival, in cooperation with the New World Symphony Orchestra, the Houston Grand Opera, with the Chicago Symphony Orchestra at Temple Sholom in Chicago and the Los Angeles Philharmonic, where it was performed in 2004 at the Wilshire Boulevard Temple.

His other Capriccio recordings include the works of Karl Amadeus Hartmann and Dmitri Shostakovich with violinist Vladimir Spivakov and the Cologne Philharmonic.

Conlon has conducted the orchestra for Kenneth Branagh's The Magic Flute (2006), a film version in English of Mozart's opera, reset during World War I, but otherwise very faithful to the original plot.