After clerking for Guy A. Bowe, the president-county judge for Schuylkill County from 1980 to 1983, Jones joined the law firm of Dolbin & Cori. When he was made a partner, the name of the firm was changed to Dolbin, Cori & Jones.
In 1986, Judge Jones began his own private practice, John Jones & Associates. He spent the next years as a trial lawyer. He also served as solicitor for several municipalities, including his hometown of Pottsville, and was a part-time assistant Schuylkill County public defender until 1995. From around 1992 until his appointment to the federal bench, Jones served as counsel to the Reading firm of Roland & Schlegel.
Jones was the chairman of the Pennsylvania Liquor Control Board from 1995 to 2002, a period marked by some controversy. He was part of a failed attempt to privatize state stores, and he banned Bad Frog Beer after determining that its label (a frog giving the finger) was in bad taste. He briefly considered running for Governor in 2001, but was appointed to fill a vacancy on the U.S. District Court for the Middle District of Pennsylvania by President George W. Bush in February 2002. He was unanimously confirmed by the U.S. Senate on July 30 and was commissioned on August 2.
After the ruling was handed down, some pundits immediately attacked it, notably Bill O'Reilly on Fox News accusing Jones of being a fascist and an activist judge. Casey Luskin and Jonathan Witt of the Discovery Institute, and activist Phyllis Schlafly, have leveled similar charges. Jones also received death threats as a result of which he and his family were given around-the-clock federal protection.
In a speech to the Anti-Defamation League on February 10, 2006 he responded to critics who claimed that he had "stabbed the evangelicals who got him onto the federal bench right in the back" by noting that his duty was to the Constitution and not to special interest groups.
In a November 2006 talk given at Bennington College, Jones again rejected the "activist judge" criticisms and explained the judiciary role and how judges decide cases:
Judge in Dover case still fighting: John E. Jones III is using the intelligent-design debate to answer his critics and talk about judicial independence.
Jun 05, 2006; Byline: Amy Worden Jun. 5--HARRISBURG -- U.S. District Judge John E. Jones III could have taken the safe route and retreated to...
A scathing decision rejects ID in Dover; Judge calls a halt to school board's "breathtaking inanity.".(NEWS)(Editorial)
Dec 23, 2005; What a wonderful Christmas gift Judge John E. Jones III has given the people of Dover, Pa.: He ruled Tuesday that the Dover Area...