The league said Cecil violated a rule that prohibits use of abusive, threatening or insulting language or gestures to game officials.
Television cameras caught Cecil using his right hand to make the gesture when officials flagged his defense for a neutral zone infraction during the second quarter Sunday. The penalty gave Denver first-and-goal, and Kyle Orton threw a 2-yard touchdown pass on the next play for a 7-0 lead.
Titans coach Jeff Fisher confirmed the fine in his Monday news conference. He called the league's punishment swift and appropriate.
"Clearly, I'm speaking on behalf of the organization that kind of conduct on the sideline, any place for that matter, is inappropriate. The league has already dealt with the issue," Fisher said.
Video of Cecil's gesture was on YouTube by halftime. Cecil declined comment after the game, a 26-20 loss in which the Titans were flagged 10 times for a season-high 111 yards in penalties. He apologized in a statement Monday night.
"I want to apologize to the NFL, organization, fans and my family for my gesture yesterday. It was inappropriate, and there is no excuse for that type of behavior under any circumstance," Cecil said.
This isn't Cecil's first fine as a coordinator.
The NFL fined him $20,000 last December when he was flagged for unsportsmanlike conduct in the Titans' Christmas night loss to San Diego. Fisher refused to share what Cecil said that drew the flag and said Cecil's comments were directed toward the Titans' staff.
Mike Pereira, the NFL's vice president of officiating from 2004-2009, wrote on Foxsports.com that Cecil accused officials of betting on the game last December. He wrote that he would suspend Cecil for his comments last year and his gesture Sunday.
Fisher said he didn't realize Cecil had made the gesture until he got into his car Sunday night. A suspension would have kept Cecil away Sunday when the Titans (2-2) visit Dallas (1-2). But Fisher said he discussed the incident with Cecil, a man fined often by the NFL when he was a hard-hitting safety in the league.
"Clearly, Chuck's an emotional individual, and it was a heat of the battle thing and he got frustrated. He understands he's got to maintain his composure, and we move on. We've moved on. He's done a nice job with the defense thus far," Fisher said.
"The defense is playing hard. They're playing aggressive, not cheap. They're playing aggressive, and they played well enough for us to win [Sunday]."
Broncos coach Jeff McDaniels said Monday the Titans' high number of penalties is a result of Fisher's coaching.
"I was proud of our team because we knew that was the kind of game it was going to be," said McDaniels, according to The Tennessean. "You can put any tape you want to of Tennessee and there's going to be 10 penalties. You either coach it or you allow it to happen. That's how I look at that.
"There's a way to play tough and physical without being excessive and playing dirty after the snap. There's a lot of teams in this league that play like that. Tough and physical but also within the rules."
Information from The Associated Press contributed to this story.