The SNP Westminster leader challenged the Prime Minister on his previous descriptions of people from Africa amid the ongoing row over racism in football.
Speaking at PMQs, Mr Blackford labelled the UK Government’s conduct as “shameful” following a failure to support England players taking the knee at Euro 2020.
He said: “The tragedy of this tournament was the undercurrent of racism that was ultimately targeted at three young men - Rashford, Sancho and Saka.
“Wherever there is racism, it falls on all of us to face it down and call it out.
“It is shameful that it took until last night for the Prime Minister to meet with the main social media companies and finally wake up to the fact that those who publish and promote vile racist abuse online need to be faced down and sanctioned.
“So, can the Prime Minister tell us what sanctions he thinks would be appropriate for someone who publishes racist content – and it shocking to even have to say this out loud -describing Africans as 'flag waving piccaninnies' with 'watermelon smiles'?”
The Prime Minister told MPs the UK Government is now changing the football banning order regime to cover online racism.
Responding, he said: “I've commented many times about the words that I've said in the past and I think the House understands how you can take things out of context.
“There is a chance now, to hold these internet companies to account, and to make sure that they face fines running to 10 per cent of their global income if they fail to take hate and racism off their platforms and I hope the Scottish National Party will support it.”
The Ross, Skye and Lochaber MP agreed but pointed out a lack of apology or explanation from the Prime Minister.
He continued: “The truth is that the Tory party don’t sanction those who publish that kind of racist content - they promote them to be Prime Minister.
"The legacy of the Prime Minister’s dog whistling has followed him into 10 Downing Street and it is now at the heart of this Tory government.
“As the England international Tyrone Mings has so powerfully stated - this government doesn’t get to stoke the fires of racism and then pretend to be disgusted by it when it happens.
“They don’t get to condemn the racism of others but deny the racism that they have provoked.
“After the shocking racism on show over the last week, does the Prime Minister still stand by his government’s belief that systemic racism is not a problem that exists in the UK?”
Mr Johnson admitted racism was a problem, but insisted his party were the “wrong target” for criticism.
He said: “This is a party that is not only had the first ever Muslim Secretary of State for Health, how was of course the former Chancellor, that has had two female Prime Ministers, the most diverse cabinet in the history of this country, and the most diverse government in the history of this country.
“If you are a young person growing up in a black or ethnic minority group in this country, we are the party that represents hope and opportunity.”