Since 1997, Miller has been the primary play-by-play voice of the San Francisco Giants (replacing Hank Greenwald), and since 1990 he has done national television and radio broadcasts of regular-season and postseason games for ESPN, most prominently alongside Hall of Famer Joe Morgan on the network's Sunday Night Baseball telecasts.

A popular and respected broadcaster, Miller has received numerous honors for his play-by-play work, including a Cable ACE Award and several Emmy Award nominations. Among his assignments to date, he has called eight World Series on ESPN Radio.

After graduating from the College of San Mateo, Miller became a Santa Rosa television sports director. In 1974, he landed his first play-by play job, calling that year's World Series champion Oakland Athletics. After one year with the Athletics and brief stints with the Texas Rangers, and the Boston Red Sox, he was hired by the Baltimore Orioles (succeeding the legendary Chuck Thompson) in 1983. In his first year in Baltimore, Miller called the Orioles' championship run:

"Everybody else is in muted silence. The pitch! Line drive! Ripken catches it at shortstop! And the Orioles are champions of the world!" - Miller calling the final out of Game 5 of the 1983 World Series.
He remained the Orioles' primary announcer through 1996, before returning to the Bay Area and joining the Giants following a contract dispute with Baltimore owner Peter Angelos, who accused Miller of not being enough of an "advocate" for the Orioles.

For a brief period in the 1970s, Miller broadcast for the California Golden Seals of the National Hockey League. He also spent the early part of his career announcing University of San Francisco basketball (1976-1980), the Golden State Warriors of the NBA (part-time, 1979-1982), and the original San Jose Earthquakes.

Jon Miller's first network exposure came in 1976, when he was selected by CBS-TV to broadcast the North American Soccer League Championship Game. From 1974-1976, Miller did play-by-play for the Washington Diplomats of the North American Soccer League. He also announced the Soccer Game of the Week for nationally-syndicated TVS from 1977-1978. From 1986-1989, Miller did backup play-by-play for NBC's Saturday Game of the Week telecasts, paired with either Tony Kubek or Joe Garagiola.

In 2003, during a game between the Giants and Arizona Diamondbacks, Miller called a play involving two defensive errors by the Diamondbacks and at least three separate baserunning mistakes by Giants outfielder Ruben Rivera. When Rivera was finally thrown out at home plate trying to score what would have been the winning run, Miller declared with mock indignation, "That was the worst baserunning in the history of the game!" The phrase was repeated numerous times on sports radio and highlight shows such as SportsCenter, and quickly became one of the most famous calls of Miller's long career.

In 1998, Miller wrote a book entitled, Confessions of a Baseball Purist: What's Right—and Wrong—with Baseball, as Seen from the Best Seat in the House (ISBN 0801863163) where he expounds on the current state of the sport.