Stein became a Hollywood consultant before he moved into acting. His film career was launched by his performance as the monotonous economics teacher in the 1986 movie Ferris Bueller's Day Off. In one scene, he gives an unscripted economics lecture, relying on his own experience in economics. The topics covered in his lecture are the Smoot-Hawley Tariff of 1930 and the then-current debate over supply-side economics. The film's director, John Hughes, told him to speak about something he knew well.[16] The only scripted lines are those in which he calls attendance, repeating "Bueller?...Bueller?" in a monotone voice.

Stein played similarly bland and unemotional characters. He had a recurring role in the TV series The Wonder Years and played himself in Dave.

He also appeared in several television advertisements, most notably for the product "Clear Eyes" throughout the 1990s and 2000s (decade) ("The difference is clear ... Clear Eyes." "Clear Eyes, wow!"). Many advertisements spoof movies of the day, such as one where Stein is a painter (a play on The Da Vinci Code). Before this, he appeared for Godfather's Pizza in 1987 and as a bland science teacher in 1990 for Sprinkled Chips Ahoy! cookies. In 2013, Stein began appearing in advertisements for small business accounting service firm 1800Accountant.