The flights are to more than 20 destinations, including four "mystery" JetBlue Getaways Vacation packages to undisclosed locations.
The three-, five- and seven-day auctions include one- and two-person roundtrip, weekend flights in September from cities including Boston, Chicago, New York, Orlando, Salt Lake City, Fort Lauderdale and Southern California.
Harlan Platt, a finance professor at Northeastern University who follows the airline industry, thinks the auctions will provide some valuable "word-of-mouth" advertising for the discount carrier.
"I think it's a great idea. In this day and age, people are inundated with ads as they are sitting on airplanes, or at airports," he said. "A subtle advertisement such as this could be very effective."
Platt said the auctions will likely produce final bids between 85 percent and 90 percent of the flight or package's total value.
"It's all about the cost of getting someone to notice you," he said. "And this (method) provides a lot of bang for the buck."
Each auction will have a specific range of dates in which customers can travel. The travel dates, times and flight numbers will be posted when the customers bid.
The vacation packages include airfare and a four-night hotel stay for two at Marriott hotels in locations including Las Vegas and Nassau, Bahamas. The four mystery packages include two locations where passports are needed and two that don't require passports.
Taxes and fees are additional and will vary according to the particular route, but they will be disclosed in each listing, according to JetBlue spokeswoman Alison Eshelman. Bidders will need to have a PayPal account.
Flights leave on Thursdays or Fridays and return on Sundays or Mondays. All travel must be completed by October 6.
Customers can access the auctions through www.jetblue.com/ebay.