William Hill is to pay a £6.2 million in penalties for "systemic social responsibility and money laundering failures", the Gambling Commission has announced.
An investigation by the body revealed that, between November 2014 and August 2016, the bookmaker breached anti-money laundering and social responsibility regulations.
It also found that senior management failed to mitigate risks and to have sufficient staff to ensure that processes for adhering to the regulations were effective.
The failures also resulted in 10 customers being allowed to deposit large sums of money linked to criminal offences which saw gains for William Hill of more than £1.2 million.
Executive director of the Gambling Commission Neil McArthur said they will use the "full range" of enforcement powers to ensure gambling is fairer and safer.
£6.2 million - penalty package William Hill has been ordered to pay for breaching rules on money laundering and social responsibility
£1.2 million - amount the bookmaker made after allowing 10 customers to deposit large sums of money linked to criminal offences
£290 million - full-year profit figure announced last month, ahead of expectations
"This was a systemic failing at William Hill which went on for nearly two years and today's penalty package - which could exceed £6.2 million - reflects the seriousness of the breaches," he said.
"Gambling businesses have a responsibility to ensure that they keep crime out of gambling and tackle problem gambling - and as part of that they must be constantly curious about where the money they are taking is coming from."
The body said some of the issues it found include the bookie not adequately seeking information about the source of punter's funds or establishing whether they were problem gamblers.
Examples of William Hill's failures include one customer being allowed to deposit £654,000 over nine months without any source fund checks being carried out.
The Gambling Commission said the customer lived in rented accommodation and was employed within the accounts department of a business - earning around £30,000 a year.
Another incident saw one person allowed to deposit £541,000 over 14 months, after an assumption based on a verbal conversation was made that their potential income could top £365,000 a year, and no further probing undertaken.
In reality, the Gambling Commission said this person was earning £30,000 a year, and was stealing from their employer to fund the habit.
As a result of the investigation, William Hill will have to pay more than £5 million for breaching regulations and divest itself of the £1.2 million it earned from transactions with the 10 customers.
The Gambling Commission also said that, where victims of the 10 customers who used cash linked to crime are identified, they will be reimbursed.
If further incidents of failures relating to the case emerge, William Hill must also strip itself of any money made from these transactions.
According to the body, the bookmaker will also have to appoint external auditors to review the effectiveness and implementation of its anti-money laundering and social policies and procedures, and share findings with the wider industry.
Responding to the news, deputy Labour leader Tom Watson tweeted: "William Hill has just been fined £6.2m by the Gambling Commission for accepting money from criminals without carrying out proper background checks.
"And this is an industry that talks about 'responsible gambling'. They're turning a blind eye to dirty money."