Dicer enzymes function at the core of RNA silencing to defend against exogenous RNA or to regulate endogenous genes. Plant DICER-LIKE4 (DCL4) performs dual functions, acting in antiviral defense and in development via the biogenesis of trans-acting short-interfering RNAs (siRNAs) termed tasiR-ARFs. These small RNAs play an essential role in the grasses, spatially defining the expression domain of AUXIN RESPONSE FACTOR3 (ARF3) transcription factors. However, contrary to tasiR-ARFs' essential function in development, DCL4 proteins exhibit strong evidence of recurrent adaptation typical of host factors involved in antiviral immunity. Here, we address how DCL4 balances its role in development with pressures to diversify in response to viral attack. We show that, in contrast to other tasiR-ARF biogenesis mutants, dcl4 null alleles have an uncharacteristically mild phenotype, correlated with normal expression of select arf3 targets. Loss of DCL4 activity yields a class of 22-nucleotide tasiR-ARF variants associated with the processing of arf3 transcripts into 22-nucleotide secondary siRNAs by DCL1. Our findings reveal a DCL1-dependent siRNA pathway that bypasses the otherwise adverse developmental effects of mutations in DCL4. This pathway is predicted to have important implications for DCL4's role in antiviral defense by reducing the selective constraints on DCL4 and allowing it to diversify in response to viral suppressors.