After graduating from the Rhode Island School of Design in 1997, he worked at Font Bureau in Boston as Senior Type Designer until founding his own type foundry, Occupant Fonts, in 2016, distributing alongside his former employers via the Type Network service.
Some of Highsmith’s most well-known typefaces are Zócalo, used by the Mexican daily El Universal, and the Antenna series, which was used in several magazine designs as well as by Ford and the official Star Wars website. Other clients for custom fonts include or have included The Wall Street Journal, Martha Stewart Living, La Prensa Gráfica of El Salvador, ESPN, and Men’s Health. His typefaces Prensa and Relay won the 2001 Bukvaːraz! award, organized by ATypI (the International Typographic Association) in 2001. In 2015, Cyrus Highsmith received the Gerrit Noordzij Prize by the Royal Academy of Art, The Hague.
In addition to typeface design, Highsmith has been teaching at his alma mater, the Rhode Island School of Design, since 2000, while also lecturing and taking part in juries in North America, Japan and across Europe. He is the author of Inside Paragraphs: Typographic Fundamentals published by Font Bureau in 2012. With his own imprint, Occupant Press, he publishes children’s books and other prints. In 2016, Highsmith founded Occupant Fonts in Providence, Rhode Island, which continues to publish his typefaces designed while at Font Bureau as well as new releases.
In September 2017, it was announced that Occupant Fonts had been acquired by the Japanese type foundry Morisawa [ja]  and thenceforth functioned as their Providence drawing office, with Highsmith as its creative director, overseeing recent RISD graduates June Shin and Cem Eskinazi. The first two releases in cooperation with Morisawa are Citrine and the Latin-character range of A1 Gothic (both derived from his typeface Allium), published that same year.
List of Typefaces
- Citrine (for Morisawa)
- A1 Gothic (latin-character range; for Morisawa)
- Antenna Serif
- Benton Sans
- Bureau Roman
- Caslon’s Egyptian
- Daley’s Gothic
- Heron Sans
- Heron Serif
- Miller Headline
- Occupant Gothic
- Salvo Sans
- Salvo Serif
Text and illustrations
- Inside Paragraphs: Typographic Fundamentals. Boston: Font Bureau, 2012. ISBN 978-0-9654-7220-3
- Apple Bear Cat. Providence (Rhode Island): Occupant Press, 2013.
- Sakomura, Hiroko. Ari Inu Usagi (Ant, Dog, Rabbit – a Japanese alphabet book). Hashima (Gifu): Bunkeido, 2016. ISBN 978-4-7999-0167-0
- Sakomura, Hiroko. Ikko Ni-hon San-biki (One Apple, Two Tulips, Three Rabbits — a book of Japanese counter words). Hashima (Gifu): Bunkeido, 2017. ISBN 978-4-7999-0224-0
- KABK, ed. Products of a Thinking Hand (Gerrit Noordzij Prize exhibition book). The Hague: Uitgeverij de Buitenkant, 2018. ISBN 978-9-4909-1382-3
- "Cyrus Highsmith". MyFonts. Retrieved 23 December 2017.
- Macmillan, Neil (2006). An A-Z of Type Designers. Yale University Press. pp. 105–6. ISBN 0-300-11151-7.
- Rawsthorn, Alice. "The Look of Letters". New York Times. Retrieved 23 December 2017.
- Middendorp, Jan. "Space and Rhythm". Eye. Retrieved 23 December 2017.
- Heller, Steven. "Rebel Without a Caslon: An Interview with Cyrus Highsmith". AIGA. Retrieved 23 December 2017.
- Palino, Christian. "An Interview with Cyrus Highsmith". Typographica. Retrieved 23 December 2017.
- Garcia, Mario R.; Reibstein, Reed. "Cyrus Highsmith: An interview with one of America's top type craftsmen". Garcia Media. Retrieved 23 December 2017.
- Middendorp, Jan. "Creative Characters: Cyrus Highsmith". MyFonts. Retrieved 23 December 2017.
- Jockin, Thomas. "Inside Paragraphs: An Interview with Font Bureau Type Designer Cyrus Highsmith". Medium. Retrieved 23 December 2017.
- "Occupant Fonts on Type Network". Type Network. Retrieved 23 December 2017.
- Devroye, Luc. "Occupant Fonts". Type Design Information. Retrieved 23 December 2017.
- "Cyrus Highsmith - Fonts In Use". Fonts in Use. Retrieved 23 December 2017.
- "Type Directors Club : News : bukva:raz! Results". 18 September 2013. Archived from the original on 18 September 2013. Retrieved 23 December 2017.
- "ATypI Bukva:raz! 2001 Award Winners". FontShop. Retrieved 23 December 2017.
- "Cyrus Highsmith receives the 2015 Gerrit Noordzij Prize - Announcements - Art & Education". www.artandeducation.net. Retrieved 23 December 2017.
- Witman, Bob. "Amerikaan krijgt Noordzijprijs". de Volkskrant. Retrieved 23 December 2017.
- "Cyrus Highsmith". www.risd.edu. Retrieved 23 December 2017.
- "Judges - Morisawa Type Design Competition 2016". competition.morisawa.co.jp. Retrieved 23 December 2017.
- "Inside Cyrus Highsmith's New Book, a Typographic Classic in the Making - Print Magazine". 5 June 2012. Retrieved 23 December 2017.
- Inc., Morisawa. "Morisawa Acquires U.S.-based Occupant LLC's All Licensed Fonts, Brand". www.prnewswire.com. Retrieved 23 December 2017.
- "Morisawa Acquires U.S.-based Occupant LLC's All Licensed Fonts, Brand". 15 September 2017. Retrieved 23 December 2017.
- "Morisawa Opens Latin Type Designing Office in U.S." Morisawa USA Inc. 9 September 2017. Retrieved 23 January 2018.
- "モリサワ 2017年の新書体を発表 (Morisawa Announces New Typefaces for 2017)". Morisawa Inc. 28 July 2017. Retrieved 23 January 2018.