Middleton's first step toward acting was signing up for a $15 acting class with friends at a California junior college. After participating in a little bit of theater in L.A., he moved to New York City to study acting. He took classes at the Herbert Berghof Studio, and Geraldine Page became his teacher.
He made his film debut in the 1983 TV movie, Miss Lonelyhearts. In 1997, Middleton wrote the one-person play, Miracle Mile, about his lifelong struggle with juvenile rheumatoid arthritis. He performed it in New York City and other parts of the US.
In the 1990s, Middleton had a recurring role on Law & Order as forensics technician, Ellis. He also played a recurring character known as Edward Markham, a rare book dealer, in the science-fiction series, Fringe. Middleton appeared as a recurring cast member on The Blacklist in which he played Glen Carter, a DMV worker who moonlights as a tracker. This is arguably his most well-known role. In 2017, he was cast as Charlie, Audrey Horne's husband, in the Showtime Network series, Twin Peaks: The Return, the sequel to the 1990s TV series, Twin Peaks.

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