John Arrillaga is one of five children born into a lower-middle-class home with his mother, Freida, and Father, Gabriel, who traced his roots to the Basque region. He attended Morningside High School in Inglewood, California and graduated in 1955. He attended Stanford University on a basketball scholarship, and was a first-team All-AAWU selection in 1960. He graduated with a bachelor's degree in geography (no longer offered) in 1960, where he was a member of Delta Tau Delta.
In the 1960s, Arrillaga and Business partner Richard Peery bought California farmland and converted it into office space. They became two of Silicon Valley's biggest commercial landlords with more than 12,000,000 square feet (1,100,000 m).
He is well known for his generous support of Stanford University. The alumni center, the Frances C. Arrillaga Building, is named in memory of his first wife, and various other athletic facilities carry his surname. In May 2006, Arrillaga gave $100 million to Stanford.
In June 2013, he again donated to Stanford, writing a check for $151 million, making it the largest individual donation in the school's history.