Soloway became interested in becoming a filmmaker while she was a student at the University of Wisconsin--Madison, and taking classes from J.J. Murphy and others in the Communication Arts program. Her time in the Women's Studies department also has shaped Soloway's artistic voice still today.
Soloway began her TV writing career on shows such as The Oblongs, Nikki and The Steve Harvey Show. She followed those shows by writing for four seasons on the HBO original series Six Feet Under, ultimately serving as co-executive producer. Six Feet Under ran from 2001 to 2005 for five seasons. She later wrote on Dirty Sexy Money, Grey's Anatomy, Tell Me You Love Me, and was executive producer/showrunner for Showtime's United States of Tara, created by writer Diablo Cody, as well as HBO's How to Make it in America, created by Ian Edelman. Soloway created the pilot Transparent for Amazon.com, which became available for free streaming and download on February 6, 2014. The program stars Gaby Hoffman, Jay Duplass, and Amy Landecker as siblings whose father (played by Jeffrey Tambor) reveals he is going through a significant life transition.
In addition to television, she has written and directed two films that have premiered at the Sundance Film Festival: Una Hora Por Favora (2012) and Afternoon Delight (2013). Afternoon Delight played at national and international film festivals and was nominated for multiple awards, including a Gotham Award for Breakthrough Performance for Kathryn Hahn, and a Spirit Award for First Feature.
Soloway is a strong supporter of feminism and also co-founded the website wifey.tv. She also co-founded the East Side Jews collective which is dedicated to "reinventing Jewish traditions and experiences in ways that would attract other young Jews largely turned off to traditional forms of religious life."
She wrote the novella Jodi K., which was published in the collection Three Kinds of Asking For It: Erotic Novellas edited by Susie Bright. Jill's memoir, Tiny Ladies in Shiny Pants: Based on a True Story, was released in hardcover in 2005, and then in paperback in 2006.