The presenter was discussing the crowd trouble at West Ham's Upton Park ground on Sky News when he said: "The sophisticated new image, the image that the England Premier League wants to portray around the world is not this.
"It was a dream for them, you know on Sunday when we saw the scenes at the King Power Stadium in Leicester, but now this is going back to the 70s and to the 80s, to everything that you were seeing that was bad about Hillsborough for instance.”
The Manchester United fan was commenting on the ugly scenes in East London which unfolded as West Ham prepared to play their last match at the Boleyn Ground after 112 years.
Kick-off was delayed until 8.30pm and Metropolitan Police officers were called to the scene after the bus was pelted with missiles.
Holmes’ comments were slammed as "crass stupidity" with calls for Sky News to order him to apologise or "relieve him of his duties immediately."
The clumsy remarks come just weeks after an inquest ruling found the 96 football fans who died in the disaster 27 years ago were “unlawfully killed.”
The jury also ruled that fan behaviour did not cause or contribute to the tragedy in what is regarded as Britain’s worst sporting disaster.
Lawyers acting for the families said the conclusions, at the end of the longest jury case in British legal history, had completely vindicated their tireless 27-year battle.
Holmes responded to the furore, seemingly blaming others for enflaming the row: "Just being made aware of someone trying to use me to stir up trouble re: The Hillsborough disaster. How low, how disgusting.
"The Hillsborough families have suffered enough without distasteful sniping like this. For the record there is no comparison between events last night at West Ham and Hillsborough. On the programme I was trying to talk about images we never ever want to see again."
But he soon took a more conciliatory tone, repeatedly apologising for the comments.
"If anyone concluded anything different my humblest and most honest apologies. I am a huge supporter of the Hillsborough struggle for justice.
"Last night's events do not remotely register in comparison.
"I am an honest and decent football supporter and man and would never seek to create such an offence. Those who are trying to do so are very wrong.
"Obviously there is no comparison between Hillsborough and the scenes at West Ham last night."
"I apologise unreservedly if anyone thought I was making that connection."
When contacted for comment, Sky News referred Huffington Post UK to Holmes' apology on Twitter.
The Holmes row will further enflame tensions between Liverpool fans and Rupert Murdoch's media empire, which part owns Sky News.
Two of Murdoch's print publications, The Times and The Sun were heavily criticised after the Hillsborough inquest after they were the only national newspapers not to feature the story on their front pages.
The Sun, in particular, sparked anger by not mentioning the inquest verdict on its front page, 27 years after its coverage accused fans of causing the disaster.
Former Liverpool players have joined supporters of the team in reigniting calls for a boycott the newspaper.
The UK’s biggest-selling newspaper has long been boycotted by a large number of people in Liverpool over its coverage of the tragedy, which it blamed hooliganism for the deaths under the front-page headline: “The Truth”.
The paper claimed Liverpool fans stole from victims, urinated on police officers and blocked rescue efforts.