He subsequently played for the Hudson Valley Renegades, the Kane County Cougars and the Charleston RiverDogs.

Dempster made his MLB debut for the Marlins, working two innings of relief, on May 23, 1998, against the Pittsburgh Pirates, allowing three earned runs on two hits in that game.

After falling to 0–3 he got his first Major League win on June 28 against the Boston Red Sox, when he allowed only 1 run in 7 innings.

On July 11, 2002, the Marlins traded Dempster to the Cincinnati Reds for Juan Encarnación, Wilton Guerrero and Ryan Snare.

[3] During spring training in 2008, Dempster's performance resulted in his being designated to the third spot on the starting rotation, with the closer job going to Kerry Wood.

[10] In May 2009 MLB indicated that the Commissioner's Office would review Dempster's up-and-in pitch to Milwaukee Brewers slugger Ryan Braun.

"[11] After reviewing the tapes, however, Major League Baseball found no wrongdoing on Dempster's part, and decided not to take any action against him.

[15] On August 18, 2013, in a game against the rival New York Yankees, Dempster was involved in a contentious incident with Alex Rodriguez.

Later, in the top of the 6th inning, Dempster gave up a home run to Rodriguez and the Red Sox lost the game 9–6.

[16] On August 20, MLB gave Dempster a five-game suspension (though he did not miss a start) and an undisclosed fine for hitting Rodriguez.

He was part of the 25-man active roster for the postseason making three relief appearances and won his first championship title when the Red Sox beat the St. Louis Cardinals in the 2013 World Series.

On February 16, 2014, Dempster announced he would not pitch or engage in any baseball activities for the entire 2014 year, stating that he wanted to spend some time with his family.

[20] On December 5, it was announced that Dempster would be taking a job in the Cubs' front office as an assistant to general manager Jed Hoyer and president of baseball operations Theo Epstein.

[24] In 2020, Dempster joined the newly launched Marquee Sports Network as a studio and game analyst for Cubs telecasts.

Dempster favored his slider over his splitter when throwing to right-handed hitters and often imparted an obvious, prolonged wiggle to his glove [26] as part of his windup, a move he claims is done in order to prevent tipping opposing batters to his pitches.

[27][28] Dempster is widely known for his laid-back attitude, constantly joking with fans and teammates, and is said to be a positive contribution to a team's clubhouse.