Meaghan Oppenheimer grew up in Tulsa, Oklahoma, and was a former child actor, working in various regional theatre productions and television shows.She graduated from Holland Hall, and then New York University—Tisch School of the Arts in 2009. Afterward, she relocated to Los Angeles to begin a screenwriting career.

In 2010, Oppenheimer wrote and starred in Hot Mess, a film about two roommates that become friends-with-benefits. She has written screenplays for a number of projects, including Fear the Walking Dead. She co-wrote the screenplay for 2015's We Are Your Friends with film maker Max Joseph.

In December of that year, ABC announced that Reese Witherspoon would be producing a new drama series for TV written by Oppenheimer, with the working title Please Don't Go, about the personal and professional life of a ruthless divorce attorney in Dallas whose past continues to haunt her. In March 2016, ABC announced that Penelope Ann Miller had been cast opposite T. R. Knight in the project that in 2016 was released as Broken—a series pilot that halted production after the first episode aired.

In 2018, Oppenheimer penned the script for the Facebook Watch TV show, Queen America.

She adapted Carola Lovering's Tell Me Lies for Hulu that was filmed and released in 2022. She also served as co-executive producer and showrunner of the series, which starred Grace Van Patten and Jackson White.