Fogelmanis began performing in musicals for his local theater at age six, performing with the Conejo Players Theatre, and began his career in television and film at age 12. He appeared in guest roles on the CBS series Partners, the Showtime series House of Lies (both 2012), and the Disney Channel series I Didn't Do It (2014). From 2014 to 2017, he starred on the Disney Channel series Girl Meets World, a spinoff of the ABC series Boy Meets World, as the eccentric and intelligent high school student Farkle Minkus, who is also the son of Boy Meets World characters Stuart Minkus and Jennifer Bassett. In December 2015, he appeared as John Darling in the play Peter Pan and Tinker Bell – A Pirates Christmas at the Pasadena Playhouse alongside Girl Meets World cast members Sabrina Carpenter and August Maturo. He also starred in the 2016 film R.L. Stine's Mostly Ghostly: One Night In Doom House.
Fogelmanis then starred in the Hazel Hayes–directed thriller miniseries PrankMe for the defunct company Fullscreen as Jasper Perkins, a social media prankster who becomes a murderer. The series premiered in September 2017. He starred as Nate in the 2018 horror film #SquadGoals and as high schooler Andy Hawkins, the love interest of protagonist Maggie (played by Diana Silvers), in the 2019 horror film Ma. For his role in Ma, he was nominated for the Teen Choice Award for Choice Summer Movie Actor. In the 11th episode of the first season of the Hulu horror anthology series Into the Dark, "School Spirit", he starred as awkward high school student Brett. He had a cameo in the Amy Poehler–directed film Moxie in 2021.
In 2022, Fogelmanis appeared as Jude Bruneau in the fourth episode of the sixteenth season of Criminal Minds. In 2023, he began starring as Nathan Walter, an openly gay teenage musician with epilepsy, in the Netflix teen drama series My Life with the Walter Boys. He starred in the 2024 Hulu horror comedy film Carved as Cody, the boyfriend of protagonist Kira (played by Peyton Elizabeth Lee). In 2022, Fogelmanis was cast in the coming-of-age film I Wish You All the Best, which was adapted from Mason Deaver's 2019 novel of the same name and was actress Tommy Dorfman's directorial debut, in the lead role of Ben DeBacker (later known in the film as B.), a non-binary high school junior who gets kicked out of their home upon coming out. The film first premiered at South by Southwest in March 2024 and was released in theaters and digitally in November 2025. Nell Minow, writing for RogerEbert.com, praised Fogelmanis's performance as "beautiful", while Luna Guthrie of Collider called it "heart-wrenching" and wrote that it displayed a "range and depth of emotion". Dennis Harvey of Variety wrote that Ben's internal conflict was not "dramatized very vividly" by Fogelmanis but that he "holds central focus strongly enough in most respects" within the film.