Cunningham's father died when Cunningham was 13, whereupon he enrolled in Girard College, the boarding school for poor orphans in Philadelphia, Pennsylvania. After graduation, he worked full-time to put himself through his home-state school, University of Delaware. He graduated from the Benjamin N. Cardozo School of Law magna cum laude in 1988.

From 1988 to 1992, Cunningham practiced corporate law with Cravath, Swaine & Moore, before taking an appointment to the law faculty at the Cardozo School of Law. He directed The Samuel and Ronnie Heyman Center on Corporate Governance, and wrote several books on value investing. From 2002 to 2007, he was Professor of Law & Business at Boston College. At that time, he received an appointment to the faculty of George Washington University where he teaches Contracts, Corporations and Law & Accounting.

Cunningham is regarded as a significant expert in the field of law and accounting, having authored some 40 scholarly articles in major law journals (including Columbia, Cornell, Michigan, Minnesota, UCLA and Vanderbilt Law Reviews) and published 10 books. His articles are widely-cited in the literature. His books are the standard teaching books for the subject of accounting in US law schools. Professor Cunningham is also one of the leading figures in developing innovative solutions to risk transfer. His proposal to use cat bond type mechanisms for transferring risk unrelated to property damage can lead to transformation of the field of alternative risk transfer.