More than 400 drivers received parking tickets on North Street between July and September, according to figures from Fife Council.
Tickets from the busy street accounted for more than 7% of the total issued in Fife, with South Street second on the list with 323 tickets issued.
Councillor Brian Thomson told the The Courier that traffic wardens were a necessity for keeping the town centre running smoothly.
He said: “One of the reasons that we need charges is because we have a lot of tourists and the town is just so busy, especially in summer.
“It does generate income of course but we need charges or it would become a free for all. Visitors would leave their cars all day and students would park all week.”
Tony McRae, a lead professional for the council, added that the number of people looking to park in St Andrews town centre meant that traffic wardens were essential.
He said: “North Street is a very busy street with high vehicle occupancy rates for its parking bays.
“There is also a high turnover of vehicles with an average of 90 minutes spent parked per vehicle in the charged areas.
“This means that over the course of a day a parking space could have several vehicles parked in it.”
Wardens issued a total of 5,698 tickets across Fife between July and September, with the potential to raise over £340,000.
Mr McRae also said: “As is the case throughout Fife if motorists obey the parking regulations then they will not receive a parking fine.”