The broadband and television operator was continuing to charge customers after services were cancelled, Comreg found.
Virgin has been told to repay 107,000 customers a total of €3m in refunds, by the telecoms regulator.
It is one of the largest cases of overbilling in Irish telecoms history, having been ongoing since 2014.
Virgin was continuing to charge customers after services were cancelled. It then failed to refund customers.
It has affected 265,000 Virgin Media broadband and television customers over the six-year period.
Virgin has until March 31 to repay the the 107,000 outstanding customers that have not had a credit applied or which have left the service. The average customer refund will be €33.
"Since June 2014 over 264,703 Virgin Media customers were charged for services beyond their cancellation date, known as post cancellation charge," according to a notice on Virgin Media's website that has been published to comply with Comreg's ruling.
"Virgin Media did not automatically refund customers that paid for charges beyond their cancellation date... Comreg's investigation found that over 141,000 customers were affected by this issue and some have been refunded. At least €2,963,895 credit on 107,185 customers’ accounts was not claimed back."
"We are committed to issuing refunds to all affected customers by the end of March 2021. If you are one of these customers be assured that Virgin Media will issue you with a full refund to the last known address by this date. For more information please call 1800 941770."
It's not the first time this year that Virgin has been in trouble over questionable billing practices. In February, Comreg found that the operator misapplied late payment fees and lost equipment fees. Virgin Media was ordered to pay customers a total of €421,000. The misapplied fees occurred between 2016 and 2017.
A spokesperson for Virgin declined to say whether the €421,000 has been repaid to customers wrongly charged for late payment fees.
However, of the €3m owed to 107,000 customers in today's overcharging case, a Comreg spokesperson said: "Virgin Media has agreed to provide specific information to verify [that Virgin will comply with the refunds order]. Comreg is satisfied that Virgin Media intends to fully co-operate to refund all affected customers."
Comreg also said the practice of retaining the credits goes against sections of the Communications Regulation Act 2002.
“Following its investigation, ComReg informed Virgin Media that it intended to seek a High Court restraining order requiring Virgin Media to cease this practice,” said the regulator.
“On the 16th of December 2020, Virgin Media provided formal commitments to ComReg which will see over €3 million refunded to affected Virgin customers. Refunds are to be paid by 31 March 2020 to more than 100,000 customers. The average refund amount due to customers that Virgin Media is refunding is €33.”
Comreg also said that Virgin Media will now review all other credits on any inactive accounts and refund those credits to customers by 30th June 2021.
“Virgin Media will not in the future allow credit to remain on closed or inactive accounts,” it said.
A Virgin Media spokeswoman said: “Virgin Media takes regulatory compliance extremely seriously and it is our position that we are in full compliance with all our regulatory obligations.
“Virgin Media has proactively co-operated with ComReg throughout this entire process and we note the investigation has now concluded.”
Virgin Media has established a dedicated helpline — 1800 941 770 — for customers to call in respect of the refund process and will publish information on its website for customers affected by the issue.