In 1983, Kawasaki got a job at Apple through his Stanford roommate, Mike Boich. He was Apple's chief evangelist for four years. In a 2006 podcast interview on the online site Venture Voice, Kawasaki said, "What got me to leave is basically I started listening to my own hype, and I wanted to start a software company and really make big bucks." In 1987 he was hired to lead ACIUS, the U.S. subsidiary of France-based ACI, which published an Apple database software system called 4th Dimension.
Kawasaki left ACIUS in 1989 to further his writing and speaking career. In the early 1990s he wrote columns that were featured in Forbes and MacUser. He also founded another company, Fog City Software, which created Emailer, an email client that sold to Claris.
He returned to Apple as an Apple Fellow in 1995. In 1998 he was a co-founder of Garage Technology Ventures, a venture capital firm that has made INVESTMENTS in Pandora Radio, Tripwire, The Motley Fool and D.light Design. In 2007, he founded Truemors, a free-flow rumor mill, that sold to NowPublic. He is also a founder at Alltop, an online magazine rack.
In March 2013 Kawasaki announced he would be joining Google as an advisor to Motorola. His role was to create a Google+ mobile device community.
In April 2014 Kawasaki became the chief evangelist of Canva. It is a free graphic-design website, for non-designers as well as professionals, founded in 2012.
On March 24, 2015, the Wikimedia Foundation announced Kawasaki had joined the foundation's board of trustees.