Alastair Majury and Robert Davies were both elected as Stirling councillors in May.
But it later emerged that Mr Majury was behind a Twitter account which likened Scottish nationalists to the Nazis.
He was suspended from the party alongside Mr Davies, who had tweeted racist jokes.
Mr Majury used his Mulder1981 account on Twitter to make derogatory remarks about Catholics, attack benefit claimants and say the SNP was too busy talking about gay marriage.
He also boasted about the size of his manhood on an online dating site.
The pair were suspended by the Scottish Conservatives on 17 May, but a spokesman for the party confirmed they had both now been readmitted.
The spokesman said: "Having served a suspension, both councillors have been readmitted to the party after offering unreserved apologies for any offence caused.
"It has been made abundantly clear that behaviour like this will not be tolerated in future."
SNP MSP James Dornan accused Scottish Conservative leader Ruth Davidson of hypocrisy over the decision to allow the two councillors to remain in the party.
Mr Dornan said: "She is keen to call out racism, sexism and other unacceptable behaviour, except when her own colleagues are the guilty ones.
"But this issue goes beyond mere hypocrisy, and exposes the ugly reality of Davidson's Tories - a party which offers a home to extremist views, turns a blind eye to prejudice and allows those who spout offensive nonsense to hold elected office."
Scottish Labour MSP Monica Lennon said it was shocking that the suspension had been lifted because the two Tories had made "racist and sectarian remarks that have absolutely no place in our society".
Green MSP Mark Ruskell, who was previously a Stirling councillor, said: "Imagine a racist and an internet troll now deciding on Stirling Council school bullying and equalities strategies."
The Lib Dems also criticised the move, which the party said had shown the "true heartlessness of the Scottish Conservatives".
Two Conservative councillors who were suspended by the party over offensive posts on Twitter have been reinstated after apologising.