Brandan Koschel marched alongside hundreds of others at the Australia Day protest through Sydney's CBD.
The 34-year-old took the stage when the march stopped and endorsed neo-Nazi views before being arrested by police.
His 40-second speech began by claiming Australian Jewish lobbies were behind controversial hate speech laws implemented after the Bondi Beach massacre.
Koschel then proceeded to incite hatred against Jews in general, according to agreed facts tendered in court.
"The Jews are the greatest enemy to this nation," he told the crowd.
"They always have been - they're an enemy to Western civilisation - and for thousands of years, Christian and Anglos, the White man has known that the Jew is our greatest enemy."
He called for the release of Joel Davis, a lieutenant of what was formerly the nation's largest neo-Nazi group, the National Socialist Network (NSN).
Davis is on remand after being charged over a call for people to "rhetorically rape" federal MP Allegra Spender.
Koschel wrapped up the speech by "heiling" white Australia and NSN leader Thomas Sewell, the agreed facts of his case say.
He wore a black shirt with a white Celtic Cross, a symbol which has been used by white supremacist groups since the 1930s.
The speech was livestreamed on YouTube and elsewhere, the court previously heard.
The 34-year-old pleaded guilty on Tuesday to one count of intentionally inciting hatred on the grounds of race.
He will face a sentence hearing at Downing Centre Local Court next Tuesday.
The NSN announced in January it would disband in anticipation of new federal laws targeting hate groups.
Davis, a key Sydney ally of Sewell, earlier told a bail hearing that he was no longer a member of the NSN and "that chapter is now closed".
Sewell faces criminal charges along with 13 other men, accused of leading an attack on Aboriginal protest site Camp Sovereignty in August.
He has not yet pleaded but told reporters that he had been provoked.
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