The cathedral city in Hertfordshire has typical asking rents of £2,307 per month.
This is 71% above the national average, according to the data by Rightmove.
It is followed by Oxford, which ranks in second place on the list of most expensive cities to rent.
The average rent in Oxford is currently £2,237 per month.
Cambridge is in third place, with average asking rents of £2,072 per month.
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The data comes as students prepare to start the new academic year, highlighting the increase in rental price growth across university cities nationwide.
St Albans is home to the University of Hertfordshire, while the other two cities ranked in the top three of the list are home to some of the most prestigious universities in the world.
The most expensive cities in which to rent contrast with Carlisle, which has the lowest rental prices in Britain.
The average rent in the cathedral city in Cumbria currently stands at £791 per month.
It means that the average rent in Carlisle is 41% below the national average.
Meanwhile, the average asking rent outside London is now a record £1,349 per month.
The annual rate of growth now stands at 5%, down from the 12% peak recorded in 2022.
Tim Bannister, Rightmove’s property expert, said: “The rental divide across Britain is clear, with an average difference of just over £1,500 between the most expensive and cheapest cities.
“Many of these cities have seen rental growth of more than 40% in the past five years, meaning it’s likely to be a significant consideration when students are thinking about where to study, and those who have already graduated working out if they can afford to stay in that city and find a job.”