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As essential calcium ion (Ca²⁺) sensors in plants, calcium-dependent protein kinases (CDPKs) function in regulating the environmental adaptation of plants. However, the response mechanism of CDPKs to salt stress is not well understood. In the current study, the wheat salt-responsive gene <i>TaCDPK27</i> was identified. The open reading frame (ORF) of <i>TaCDPK27</i> was 1875 bp, coding 624 amino acids. The predicted molecular weight and isoelectric point were 68.905 kDa and 5.6, respectively. <i>TaCDPK27</i> has the closest relationship with subgroup III members of the CDPK family of rice. Increased expression of <i>TaCDPK27</i> in wheat seedling roots and leaves was triggered by 150 mM NaCl treatment. TaCDPK27 was mainly located in the cytoplasm. After NaCl treatment, some of this protein was transferred to the membrane. The inhibitory effect of <i>TaCDPK27</i> silencing on the growth of wheat seedlings was slight. After exposure to 150 mM NaCl for 6 days, the NaCl stress tolerance of <i>TaCDPK27</i>-silenced wheat seedlings was reduced, with shorter lengths of both roots and leaves compared with those of the control seedlings. Moreover, silencing of <i>TaCDPK27</i> further promoted the generation of reactive oxygen species (ROS); reduced the activities of superoxide dismutase (SOD), peroxidase (POD) and catalase (CAT); aggravated the injury to photosystem II (PS II); and increased programmed cell death (PCD) in wheat leaves under NaCl treatment, confirming that the <i>TaCDPK27</i>-silenced seedlings exhibited more NaCl injury than control seedlings. Taken together, the decrease in NaCl tolerance in <i>TaCDPK27</i>-silenced seedlings was due to excessive ROS accumulation and subsequent aggravation of the NaCl-induced PCD. <i>TaCDPK27</i> may be essential for positively regulating salt tolerance in wheat seedlings.