Deputy council leader Jacob Taylor said: “This leaves a large unpaid amount to the city council, which will have an impact on the overall budget.
“I think it is important that the council and the city reflects on the decisions that have led us to this point – and learn lessons for the future.”
In 2014, the council agreed to lend £36.2m to Brighton i360 Ltd to fund the 531ft (162m) tower – money which came from the government’s Public Works Loan Board.
In December last year, council leader Bella Sankey said the company had paid £250,000 towards that year’s debt, but the annual total should have been £1.49m, with payments due each June and December.
In January this year, the i360 had repaid £5.8m. However, under its original repayment schedule, it had been due to pay almost £18m by September 2023.
The council said the £51m debt consisted of the council loan at a commercially agreed interest rate, and the £4m Coast to Capital loan.
The last payment to the council was made in June 2023.
“The actual loss to the council relates to the underlying loan debt and interest repayable to government which stands at c. £32m,” the council said.