The extremist group, whose leaders were jailed last year, sent an email to subscribers claiming “thousands” of its activists were becoming members of the Tories.
It came after Mr Johnson was endorsed by Tommy Robinson and garnered public support from other far-right figures.
“If you haven’t joined the Conservative Party yet, we urge you to do so immediately, to make Boris Johnson’s leadership more secure,” Britain First said in an email sent on Wednesday.
“Senior Britain First officials and rank-and-file members have been receiving their Conservative membership cards in the post.
“Just as Momentum activists joined the Labour Party to solidify Jeremy Corbyn’s grip on that party, Britain First activists and members seem to be doing the same for the Tories and Boris.”
The group published a photograph of a Conservative Party membership card said to belong to its chief of staff, Andrew Edge.
It appeared to show he had joined in the Hazel Grove constituency in Greater Manchester, which is represented by William Wragg.
Britain First public relations officer Ashlea Simon, who was recently among senior figures investigated by counterterror police, claimed Mr Edge had been “out campaigning for them all along as well”.
In a poll on the encrypted Telegram app, 43 per cent of respondents on Britain First’s channel said they had joined the Conservatives.
The group, formerly a political party founded by ex-British National Party members, became notorious for carrying out “Christian patrols” and storming mosques.
In March 2018, leader Paul Golding and his former deputy Jayda Fransen were jailed for religiously aggravated harassment.
Britain First gained international notoriety when Donald Trump shared several of Fransen’s anti-Muslim Twitter posts in 2017, sparking a diplomatic row after Theresa May condemned the actions.
Its Facebook page was “liked” by more than 2 million people before it was deleted, while Twitter has also taken action against the group.
Britain First is the latest far-right group to endorse the prime minister, who has earned support among nationalists for his pledge to “get Brexit done” and comments comparing Muslim women to letterboxes.
Tommy Robinson declared that “everyone should vote for Boris Johnson” in the election and posed wearing a mask of the prime minister’s face as the results came in.
The English Defence League founder previously called on his followers to “back Boris” and characterised him as a champion “for the people” versus “traitors in parliament”.
Former Liberal Democrat leader Jo Swinson, who lost her seat last week, wrote to Mr Johnson saying that Robinson’s “endorsement should be anathema to any candidate seeking to improve the lives of people across the UK”.
At the time, a spokesperson for Mr Johnson told The Independent: “The prime minister is clear that divisive politics has no place in our society and does not condone the views of Robinson.”
The Muslim Council of Britain (MCB) said Downing Street’s response did not go far enough.
“The prime minister must reflect on whether his party’s attitude towards Muslims and inaction on Islamophobia may have played a role in such endorsements,” secretary general Harun Khan told The Independent.
Mr Johnson originally promised an independent inquiry into Islamophobia in the party when he was campaigning to become leader, but the commitment has been widened to cover all forms of discrimination and prejudice.
The Conservative Party said Professor Swaran Singh would look at how it could improve its procedures and ensure “any instances are isolated and that there are robust processes in place to stamp them out”.
It came after Mr Johnson apologised for “all the hurt and offence” that had been caused to the Muslim community after a succession of scandals over comments by election candidates and politicians.
The prime minister has dismissed warnings that his language could inflame tensions and attacks on MPs as “humbug” in parliament, after repeatedly calling a law preventing a no-deal Brexit a “surrender act” and claiming the opposition wanted to “betray the people”.
Experts have said Mr Johnson had been “using the language of the far right” and playing into extremist narratives.
Chloe Colliver, who leads the digital research unit at the Institute for Strategic Dialogue think-tank, said Mr Johnson was “calling successfully to a nationalist interpretation of the Brexit debate”.
“It seems very purposeful to me and it really harks back to the Second World War nostalgia in this debate, which plays powerfully to the far right and nationalist groups,” she previously told The Independent.
Police leaders have repeatedly called for politicians and other public figures to avoid worsening tensions around Brexit with inflammatory language.