Fay Jones, the Tory candidate for Brecon & Radnorshire, said Mr Johnson was wrong to respond to the incident by making political points after two people were killed in the stabbing attack on Friday.
The father of one of he victims, David Merrit, issued statements condemning the use of the attack for "political gain".
But the prime minister provoked criticism when he attacked Labour over the release of convicted terrorist Usman Khan and for writing an opinion piece under the headline “Give me a majority and I'll keep you safe from terror”.
“I don’t think we should be making politics out of this,” Ms Jones said during a BBC Wales Live election debate on Tuesday.
“I don’t think the prime minister or anyone should be using this as a political exercise.”
The Tory candidate originally gave her criticism in general terms and argued that “both sides” had been involved in a “blame game” over the attack.
After a series of audience comments criticising Mr Johnson, she was asked explicitly if the prime minister was wrong.
“Yes, he was,” Ms Jones replied.
The Conservative Party did not respond to a request for comment in time for publication.
Mr Johnson was also condemned by the other candidates in the debate, with Labour’s David Hanson saying police had struggled with funding cuts and the Lib Dems’ Steffan John saying Mr Johnson “played games” on the issue.
The London Bridge attacker was released from prison in 2018 on licence after serving time for terrorism offences, raising questions about why he was allowed out of prison when he still posed a threat to the public.
The prime minister has argued that he has campaigned against early release and short sentences for many years and blamed Khan’s release on the “leftie” Labour government before 2010.
However, critics have challenged Mr Johnson on what the Conservatives have done in the past decade to address the issue.
Labour leader Jeremy Corbyn called for a full investigation into the criminal justice system after last week’s attack and said there were “urgent” questions to answer about Khan’s release.
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