Nuclear genome in plants harbors thousands of genes encoding protein targeting to cytoplasmic plastid and/or mitochondria (hereafter abbreviated as NTCGs which enclose Chlo.-NTCGs and Mit.-NTCGs). It is established that many NTCGs are generated by ancient gene transfer from endosymbiotic ancestors (cyanobacteria and proteobacteria) of foregoing organelles (abbreviated as NUPT and NUMT, respectively). In addition, some other NTCGs have organelle-targeting transit peptide encoded in their mature protein while they were non-symbiotic origin (not inherited from either symbiotic ancestor). The evolutionary path and functional necessity of those NTCGs via NUMT and NUPT have been extensively explored; however, it is underexplored about the evolution dynamics of NTCG profiles and potential function implications for their composition variation in specific evolutionary process. Accordingly, within Triticum/Aegilops complex, we focused on the evolution of non-symbiotic NTCGs in diploid speciation, allotetraploid domestication, allohexaploidization, allohexaploid improvement, and allohexaploid de-domestication processes. We found that: (i) within respective diploid speciation, non-symbiotic species-specific Chlo.-NTCGs and Mit.-NTCGs in T. urartu and Ae. speltoides were more abundant than other species in the same species complex; (ii) unique genomic loss and gain of non-symbiotic species-specific Chlo.-NTCGs and Mit.-NTCGs contribute to foregoing evolutionary dynamics in most extent; (iii) within allotetraploid domestication, both A- and B-subgenomic non-symbiotic NTCGs displayed the overall loss of organelle-targeting ability; however, the latter loss of organelle-targeting ability in B-subgenome (maternally contributed) was less than that in former A-subgenome. Similar trend was observed in allohexaploid improvement as well; (iv) supportively, within allohexaploid de-domestication in the opposite direction from domestication and improvement, both A- and B-subgenomic non-symbiotic NTCGs displayed the overall gain of organelle-targeting ability, which was more significant for B-subgenomic non-symbiotic NTCGs; (v) within allohexaploidization, more non-symbiotic D-subgenomic NTCGs obtained organelle-targeting ability than other non-symbiotic subgenomic NTCGs did. Our findings provide unique and novel insights into the evolution of NTCGs and the functional co-evolution between nuclear and organellar genomes.