Seacrest began his career in 1990 at age 15 with Atlanta radio station WSTR/Star 94 FM while still in high school by interning with nighttime personality Tom Sullivan. Sullivan trained Seacrest in all aspects of broadcasting and put him on the air for the first radio broadcast of his career. He made his first television appearance in 1993, hosting the Radical Outdoor Challenge.

In 1995, Seacrest became the afternoon drive DJ at "Star 98.7" (KYSR-FM), an adult contemporary radio station in Los Angeles, California. Despite all of his other projects, he remained committed to that DJ role until 2003. Also during his early twenties, Seacrest hosted a few short-lived game shows. His first TV gig was Gladiators 2000 for syndication and Wild Animal Games for Fox Family (now ABC Family). In 1997, Seacrest hosted the weekly syndicated internet game Click, which lasted only two seasons. Also from time to time he became a substitute host for E!'s Talk Soup.