In 1972, he moved to New York City, where he secured several television commercials and appeared in off Broadway plays. He was eventually cast as Dale Robinson in the daytime drama Somerset. He later created the original Brad Vernon on One Life to Live.
Parker made his motion picture debut in The Bell Jar and also starred in 1980's A Small Circle of Friends, where he played one of three radical college students during the 1960s. The United Artists-released film received only a limited theatrical release, ultimately grossing under $1 million.. Another film to his early acting career was the controversial White Dog.
Parker has guest-starred on the ABC series Family and Hart to Hart, Walker, Texas Ranger, and such TV movies as Who is Julia, Dead Before Dawn and Violation of Trust. He appeared on Major Dad and American Justice with his Simon & Simon former co-star Gerald McRaney.
During his hiatus from Simon & Simon, Parker co-produced and co-starred in an action adventure feature film shot on location in Arizona. After completing his movie, he returned to his alma mater, Beloit College, to star in a live summer stock theatrical production, playing Brick in Cat on a Hot Tin Roof.
In his book An Accidental Cowboy, Jameson Parker recounts his life after Simon & Simon. Another book Parker has written is called To Absent Friends, which he calls "a collection of stories of the dogs we miss".
Parker has often stated that he was not the typical "Hollywood type", and that he is very much a homebody.
In the fall of 1992, Parker suffered a gunshot wound near his condo, the result of a dispute with his neighbor. Parker made a full recovery, and the neighbor was charged for attempted murder, sentenced to nine years in prison.