He lived for a time with his maternal grandfather, David DeWitt, an IBM Fellow, who played a large part in introducing Dayton to technology.

Dayton transitioned his title from founding CEO to executive chairman, handing over day-to-day operations of the company to Charles "Garry" Betty.

[25] A long-time Mac user, Dayton led the creation of a strategic partnership with Steve Jobs at Apple in 1998 that made EarthLink the default ISP pre-loaded on the iMac.

[8] In 2005, Dayton became CEO of Helio, a mobile phone joint venture of EarthLink and SK Telecom, formed with $220 million in funding from each company.

[47] He is an investor in and board member of Diffbot,[48][49] a semantic web and structured data startup,[50] and Artsy,[51][52] an online art marketplace, which raised a reported $50 million in July, 2017.

"[54] He is an investor in Joby Aviation, a NASA LeapTech participant building an electric vertical take-off and landing aircraft, which raised $100 million[55][56] from Intel, JetBlue and Toyota in February, 2018 and went public in August, 2021, at a value of $6.6 billion.

[57][58] Dayton was an early investor in video doorbell company Ring,[59] which was acquired by Amazon in February, 2017 for $1 billion[60] Dayton is a co-founder of City Storage Systems and CloudKitchens, which in March, 2018 secured a $150 million investment from Uber founder Travis Kalanick, who also joined the company as its CEO,[61][62] with plans as of February, 2019, to expand into China.

[63][64] City Storage Systems buys "distressed" properties and converts them into spaces equipped for online retail, specifically food delivery.

[65] In January, 2019, Dayton led the Series A investment in micro satellite startup Swarm Technologies, along with PayPal co-founder David Sacks.

About the investment, Dayton said, “Swarm’s approach reminds me of the early years at EarthLink—stay super scrappy, serve customers and generate revenue quickly.”[66] Swarm was acquired by SpaceX in August, 2021,[67] in a transaction described as "a rare deal by Elon Musk’s space company that expands the team — and possibly the technological capabilities — of its growing Starlink internet service.

[72] In a March 2023 interview with Fox Business, Dayton pointed to the ever-increasing demand for more pilots and noted, “...we’re not going to solve it with traditional technology” and that he believed new VR simulators could provide “...training that is equivalent to flying in the actual aircraft...[at] a tenth to a twentieth the cost.”[73] In Walter Isaacon’s biography Elon Musk, Dayton is referred to as a “fellow libertarian”.

[74] Dayton has listed authors Henry Hazlitt, Frederic Bastiat, and Ayn Rand as significant influences, stating, “It never occurred to me to go to the government for a solution.

[79] In 2007, Dayton served on the advisory board of the Center for Public Leadership at the John F. Kennedy School of Government at Harvard University.