Raised in Connecticut, Cunningham graduated from Franklin & Marshall College before earning an MFA from Stanford University.

After completing his education, he worked as a manager for various theater companies, including New York City's Lincoln Center and the Oregon Shakespeare Festival.

While working for a documentary company in New York, Cunningham made his feature film directorial debut with The Art of Marriage (1970).

While working for a documentary company in New York City in the late 1960s, Cunningham made his directorial debut with The Art of Marriage (1970).

Cunningham is best known for his involvement of multiple films in the Friday the 13th franchise, which introduced the fictional mass murderer Jason Voorhees.