He started his law career in New York with the firm now called Cravath, Swaine & Moore, where he met his future partner Lloyd N. Cutler.
He then served for two years as a law clerk to Justice Frank Murphy of the United States Supreme Court, a former governor of Michigan known as a defender of civil liberties.
Over time, the firm opened offices in London, Brussels, Berlin, and New York and grew to several hundred lawyers.
John Pickering was remembered by his colleagues as an exceptional mentor who always took a personal interest in young lawyers and staff.
His pro bono work involved civil rights in Mississippi, doctor-assisted suicide, affirmative action in admissions at the University of Michigan, the financing of legal services for the poor, the rights of the elderly, and the House's expulsion of Representative Adam Clayton Powell Jr., Democrat of New York.