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In 2006, D'Esposito joined Marvel Studios, making his debut as unit production manager and executive producer on Iron Man (2008). He continued in these roles on Captain America: The First Avenger and various Marvel One-Shots. Over time, he became a central figure in the Marvel Cinematic Universe's growth, executive producing virtually every MCU film since Iron Man (with the sole exception of The Incredible Hulk) and guiding franchises including Captain America, Guardians of the Galaxy, Black Panther, and Avengers, collectively earning over $29 billion at the global box office.

Beyond production, D'Esposito has directed Marvel One-Shots—Item 47 (2012) and Agent Carter (2013)—the latter laying the groundwork for the Agent Carter TV series.

He advanced to co-president of Marvel Studios in 2009, sharing leadership with Kevin Feige. In that capacity, he oversees feature film and streaming series development and production, including titles like WandaVision, The Falcon and the Winter Soldier, Loki, Ms. Marvel, Ironheart, Your Friendly Neighborhood Spider-Man, Daredevil: Born Again, and numerous other projects.

He has received Primetime Emmy nominations for WandaVision in 2021 (Outstanding Limited or Anthology Series) and for What If…? in 2022 (Outstanding Animated Program). In 2024, he was nominated for Outstanding Animated Program again for X‑Men ’97 (Season 1 Episode 5, “Remember It”). Additionally, he earned nominations from the Television Academy for The Falcon and the Winter Soldier, Loki, and Echo in technical categories, including costumes, sound mixing, and visual effects. Beyond industry awards, he was honoured in January 2024 with the inaugural “Renaissance Award” from the Russo Brothers’ Italian American Filmmaker Forum in recognition of his contributions to Italian‑American heritage and the entertainment world.