He briefly attended the University of Alberta where he had applied for both mathematics and music. He was rejected by the music program, and then went on to study mathematics and received his Bachelor of Science (B.S.) degree from the University of British Columbia in 1973.

Cheriton received his Master of Science (M.S.) and Doctor of Philosophy (Ph.D.) degrees in computer science from the University of Waterloo in 1974 and 1978, respectively. He spent three years as an assistant professor at his Alma mater, the University of British Columbia, before moving to Stanford.

In 1980, Cheriton married Iris Fraser. They had four children, and divorced in 1994.

Cheriton cofounded Granite Systems with Andy Bechtolsheim. The company developed gigabit Ethernet products. It was acquired by Cisco Systems in 1996.

In August 1998, Stanford students Sergey Brin and Larry Page met Bechtolsheim on Cheriton’s front porch. At the meeting, Bechtolsheim wrote the first cheque to fund their company, Google, and Cheriton joined him with a $200,000 investment.

In 2001 Cheriton and Bechtolsheim founded another start-up company, Palo Alto based Kealia. Kealia designed a high-capacity streaming video server; Galaxy, a range of servers based on AMD’s Opteron microprocessor; and Thumper, an enterprise-grade network attached storage system. Kealia was bought by Sun Microsystems in 2004, with Thumper becoming the Sun Fire X4500.

Cheriton founded and led the Distributed Systems Group at Stanford University, which developed a [[microkernel] operating system named V. He has published profusely in the areas of distributed computing and computer networking. He won the prestigious SIGCOMM award in 2003, in recognition for his lifetime contribution to the field of telecommunications networks. Cheriton was the mentor and advisor of students such as: Sergey Brin and Larry Page (founders of Google), Kenneth Duda (founder of Arista Networks), Hugh Holbrook (VP Software Engineering at Arista Networks), Sandeep Singhal (was GM at Microsoft, now at Google), and Kieran Harty (CTO and founder of Tintri).

Cheriton was also an early angel investor in compute virtualization leader VMware, which was later acquired for $625M by EMC in 2004. VMware had a successful public offering in 2007.

In 2004, Cheriton cofounded (again with Bechtolsheim) and was chief scientist of Arista Networks, where he worked on the foundations of the Extensible Operating System (EOS). Arista had a successful public offering in 2014.

On November 18, 2005, the University of Waterloo announced that Cheriton had donated $25 million to support graduate studies and research in its School of Computer Science. In recognition of his contribution, the school was renamed the David R. Cheriton School of Computer Science. In 2009, he donated $2 million to the University of British Columbia, which will go to fund the Carl Wieman Science Education Initiative (CWSEI). He more recently donated $7.5M to fund a new chair in computing, and a new course on computational thinking.

Cheriton is an investor in and advisory board member for frontline data warehouse company Aster Data Systems, which was acquired by Teradata in 2011 for $263M.

In 2014, Cheriton cofounded and invested in Apstra, Inc. In 2015, he cofounded and invested in BrainofT, Inc. (Caspar).

As of 2016, Cheriton is working with Stanford students on transactional memory, making memory systems that are resilient to failures.

According to public record, Cheriton made a total of over $5,000 donations to the presidential candidate Donald Trump in 2019.