After his departure from MST3K, Conniff went on to become executive story editor for the popular ABC series Sabrina, the Teenage Witch. He made a few on-air appearances on the show, most notably as "Rootie Kazootie", a baby-turned-adult due to Sabrina's wishing spell.
He later showed up as a writer and later as head writer on the ill-fated Nickelodeon animated TV series Invader Zim, even providing some voices before departing from that show as well, marking the second TV show that he has been associated with that was cancelled due to conflicts with station management over content and creative direction, and the second show that achieved cult status following its cancellation. In the summer of 2005 Conniff provided the voice for legendary cowboy Buffalo Bill Cody in two episodes of The Radio Adventures of Dr. Floyd.
Frank was the host of Cartoon Dump, a monthly comedy/music revue that ends by showcasing some of the worst cartoons of all time, at the Steve Allen Theatre in Los Angeles. Fellow MST3K alum Joel Hodgson joined the cast, creating his own puppet, "Dumpster Diver Dan." Cartoon Dump is available as a podcast on http://www.cartoonbrewfilms.com.
As of 2019, Frank Conniff performs with Trace Beaulieu as "The Mads" in several capacities, including a podcast and a traveling live show. They appeared together (along with many of their former castmates) at the special live MST3K Reunion show put on by RiffTrax in 2016. Frank and Trace also performed on the tag-team RiffTrax production for Batman v Superman: Dawn of Justice (which also included Mary Jo Pehl).
During the 2020 livestream of The Mads riffing of Glen or Glenda, viewers could see posters from Cinematic Titanic on the walls of Frank's home.