Emanuel made the announcement Tuesday morning from the CTA stop at the Merchandise Mart.
Claypool made an unsuccessful bid against Joe Berrios to be Cook County assessor in November.
He has been serving as a member of Emanuel's Transportation and Infrastructure transition team.
"He has been a passionate advocate for mass transit and public transit. He shares my belief that it is our most critical piece of infrastructure. Forrest has the experience to capitalize on the CTA's strengths and the creative mind to guide its future," Emanuel said.
Though Claypool, a longtime political friend of Emanuel, has no experience running a public transit agency, the mayor-elect says Claypool brings other attributes to the job.
"It's bringing innovation, creativity, a sense of commitment to what the mission is. And that is why I selected him," said Emanuel.
The one-time Daley administration chief of staff served as Chicago parks superintendent in the 1990s. Claypool also has worked for and with David Axelrod, a political consultant for Emanuel and President Barack Obama.
One of Claypool's first challenges at the deficit-ridden CTA will be to negotiate new labor contracts.
"Obviously, there are significant financial problems at the CTA, but that's part of the discussions and the negotiations," said Claypool.
Transit advocate Ron Burke of the Active Transportation Alliance praised Emanuel's choices, but said the verdict is still out on Claypool.
"I think we'll all have to wait and see just how well he can perform in this job. We're not going to just assume that he's going to be good at it. But we are optimistic," said Burke.
Claypool replaces Daley appointee Rich Rodriguez who won praised for the CTA's performance during last winter's blizzard. Emanuel did not rule out a place for Rodriguez in his administration.
"I also have asked Mr. Rodriguez to maybe serve in other parts of the administration so he can bring his experience," said Emanuel.
Claypool is not the first CTA president with no prior public transit experience. Rodriguez and his predecessor, Ron Huberman, were also public transit neophytes when they were appointed by Mayor Daley.
Emanuel on Tuesday also announced that he is keeping Terry Peterson on as chairman of the CTA Board. Peterson is a longtime ally of current Mayor Richard Daley and a former 17th Ward alderman and Chicago Housing Authority boss. Emanuel also appointed Gabe Klein as the new Chicago Department of Transportation commissioner. He worked as director of the District Department of Transportation in Washington.
"Gabe will build on our system's strengths. He's results driven and will work with the rest of my leadership team to make Chicago a model of livability for residents so that everyone has access to good transportation options, good jobs and a good education," Emanuel said.
On Monday, Emanuel named Rochester, N.Y., school superintendent Jean-Claude Brizard as his pick to lead Chicago Public Schools.