diff --git a/src/nvim/api/command.c b/src/nvim/api/command.c
index 4b334d3e3b..cc5031d7be 100644
--- a/src/nvim/api/command.c
+++ b/src/nvim/api/command.c
@@ -726,6 +726,7 @@ String nvim_cmd(uint64_t channel_id, Dict(cmd) *cmd, Dict(cmd_opts) *opts, Arena
 
   garray_T capture_local;
   const int save_msg_silent = msg_silent;
+  const bool save_redir_off = redir_off;
   garray_T * const save_capture_ga = capture_ga;
   const int save_msg_col = msg_col;
 
@@ -737,6 +738,7 @@ String nvim_cmd(uint64_t channel_id, Dict(cmd) *cmd, Dict(cmd_opts) *opts, Arena
   TRY_WRAP(err, {
     if (opts->output) {
       msg_silent++;
+      redir_off = false;
       msg_col = 0;  // prevent leading spaces
     }
 
@@ -747,6 +749,7 @@ String nvim_cmd(uint64_t channel_id, Dict(cmd) *cmd, Dict(cmd_opts) *opts, Arena
     if (opts->output) {
       capture_ga = save_capture_ga;
       msg_silent = save_msg_silent;
+      redir_off = save_redir_off;
       // Put msg_col back where it was, since nothing should have been written.
       msg_col = save_msg_col;
     }
diff --git a/src/nvim/api/vimscript.c b/src/nvim/api/vimscript.c
index fc7e7e1a06..1c74d5d985 100644
--- a/src/nvim/api/vimscript.c
+++ b/src/nvim/api/vimscript.c
@@ -72,6 +72,7 @@ Dict nvim_exec2(uint64_t channel_id, String src, Dict(exec_opts) *opts, Error *e
 String exec_impl(uint64_t channel_id, String src, Dict(exec_opts) *opts, Error *err)
 {
   const int save_msg_silent = msg_silent;
+  const bool save_redir_off = redir_off;
   garray_T *const save_capture_ga = capture_ga;
   const int save_msg_col = msg_col;
   garray_T capture_local;
@@ -83,6 +84,7 @@ String exec_impl(uint64_t channel_id, String src, Dict(exec_opts) *opts, Error *
   TRY_WRAP(err, {
     if (opts->output) {
       msg_silent++;
+      redir_off = false;
       msg_col = 0;  // prevent leading spaces
     }
 
@@ -92,6 +94,7 @@ String exec_impl(uint64_t channel_id, String src, Dict(exec_opts) *opts, Error *
     if (opts->output) {
       capture_ga = save_capture_ga;
       msg_silent = save_msg_silent;
+      redir_off = save_redir_off;
       // Put msg_col back where it was, since nothing should have been written.
       msg_col = save_msg_col;
     }
diff --git a/test/functional/api/vim_spec.lua b/test/functional/api/vim_spec.lua
index abcefd28bf..81f1da8109 100644
--- a/test/functional/api/vim_spec.lua
+++ b/test/functional/api/vim_spec.lua
@@ -385,6 +385,9 @@ describe('API', function()
       )
       eq({ output = '' }, api.nvim_exec2('echo', { output = true }))
       eq({ output = 'foo 42' }, api.nvim_exec2('echo "foo" 42', { output = true }))
+      -- Returns output in cmdline mode #35321
+      feed(':')
+      eq({ output = 'foo 42' }, api.nvim_exec2('echo "foo" 42', { output = true }))
     end)
 
     it('displays messages when opts.output=false', function()
@@ -4945,6 +4948,9 @@ describe('API', function()
 
     it('captures output', function()
       eq('foo', api.nvim_cmd({ cmd = 'echo', args = { '"foo"' } }, { output = true }))
+      -- Returns output in cmdline mode #35321
+      feed(':')
+      eq('foo', api.nvim_cmd({ cmd = 'echo', args = { '"foo"' } }, { output = true }))
     end)
 
     it('sets correct script context', function()