After attending summer acting camp at age 7, Whelan landed a series of commercials. At age 11, she was cast in the short-lived TV series Friends (a little-known 1979 series). Later that year, Whelan played the role of Lisa Davis, the sick girl, in Airplane! After The Love Boat was canceled in 1986, she worked on an album titled Our Time. During the early 1980s, Whelan served as a national spokeswoman for First Lady Nancy Reagan's "Just Say No" anti-drug campaign. She later took a role on the long-running TV soap opera The Young and the Restless.
On November 25, 2001, Whelan appeared on an episode of The Weakest Link, a trivia game show hosted by Anne Robinson. Whelan competed against other celebrity TV stars, including Mackenzie Phillips, Nell Carter, Cindy Williams, Joan Van Ark, Erin Moran, Erik Estrada, and Fred "Re-run" Berry. She outlasted the others, winning $57,000 for her charity.
On September 10, 2008, Whelan appeared with several other cast members from the movie Airplane! in a reunion segment on NBC's the Today Show. In October 2008, Whelan made her New York City cabaret debut with her one-woman show Jill Whelan: An Evening In Dry Dock at The Metropolitan Room. From September to November 2011, Whelan appeared in the British farce Move Over Mrs. Markham at Stage West Theatre Restaurant in the Toronto, Ontario area.
Whelan was set to replace Mark Thompson, who retired on August 17, 2012, after 25 years co-hosting The Mark & Brian Show on KLOS in Los Angeles, but during Thompson's final broadcast, co-host Brian Phelps announced that he, too, was quitting KLOS. Jill met her partner, Brian Phelps, over 20 years ago and the two have wanted to work together ever since. Phelps and Whelan are instead co-hosting a comedy podcast at www.brianandjillshow.com. Whelan and Phelps share a love for improvisational comedy, and have created hundreds of characters together that they have performed both on the stage during improv shows and now in sketches performed on their podcast.
After returning to the United States from college, Whelan moved to New York City and acted in several Off-Broadway productions before leaving the stage to work as an event producer at Madison Square Garden, where she met her second husband, whom she married over a decade later. Whelan met her first husband, Brad St. John, shortly after leaving Madison Square Garden; soon after their wedding, she became pregnant with their first son, Harrison. After The Young and the Restless, she left acting and started working as an investigative producer at the Los Angeles television station KCOP, where she remained for four years before moving back to the East Coast to get married again. She married her second husband, John Chaykowsky in April 2004 aboard the cruise ship Caribbean Princess. Her second son, Grant, was born in 2006. In 2014 according to media reports, Whelan filed for divorce from Chaykowsky.
At some unknown point in time, she lived in Yardley, Pennsylvania, where she hosted a Sunday afternoon radio show on WPHT 1210 AM in Philadelphia. The show aired Sunday from 3 pm to 4 pm. Additionally, Whelan taught acting to children and teens.
Whelan moved back to Los Angeles in 2012, where she lives and raises her two sons.