The 21-year-old left-back featured in the Terriers' successful Championship play-off campaign in May and started seven league games last season.
Holmes-Dennis has previously spent time on loan at Oxford United, Plymouth Argyle and Oldham Athletic.
"This allows me to get games and challenge myself," he told BBC Radio Solent. "It's a chance to show myself."
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Portsmouth have signed Huddersfield Town defender Tareiq Holmes-Dennis on a season-long loan deal.