Wolfhard was born on December 23, 2002, in Vancouver, British Columbia, Canada, to a family of French, German, and Jewish descent.

[10] He and co-stars Noah Schnapp, Gaten Matarazzo, and Caleb McLaughlin competed against one another in a 2017 episode of Spike's Lip Sync Battle.

[11] In July 2017, Wolfhard co-directed his first music video with Josh Ovalle for the band Spendtime Palace's song "Sonora".

[19] He played Tyler, an altruistic and thoughtful pizza delivery boy, in the 2018 Ken Marino-directed ensemble comedy film, Dog Days.

[20] In January 2019, Wolfhard starred in the Netflix animated series Carmen Sandiego as "Player", the title character's chief accomplice and friend.

Wolfhard joined the Jason Reitman–directed comedy miniseries Home Movie: The Princess Bride, which raised money for World Central Kitchen,[38] and performed a live reading of The Princess Bride's script, as the Grandson, for a Democratic Party of Wisconsin charity event in September 2020.

[44] The audiobook was adapted by Eisenberg into the comedy-drama film When You Finish Saving the World (2022), with Julianne Moore and Wolfhard starring as mother and son.

[48][49][50] He was cast alongside Willem Dafoe, Emily Watson, and Helena Zengel in A24's fantasy epic The Legend of Ochi, directed by Isaiah Saxon.

[54] In 2023, Wolfhard and his friend and frequent collaborator Billy Bryk released the theatrical feature film Hell of a Summer, which they co-directed, co-wrote and co-starred in.

[57] That same year, he voiced a younger version of the titular character in Scott Pilgrim Takes Off, released in November.

[58] A few weeks later, it was announced that Wolfhard's new band, The Aubreys, with Calpurnia drummer Malcolm Craig, would debut on the soundtrack of his film, The Turning (2020).

[66] In May 2017, Wolfhard hosted "Strange 80s," a benefit concert to raise funds for Sweet Relief, an organization that helps struggling musicians in need of medical care.