diff --git a/Cargo.toml b/Cargo.toml
index ff1c1e00176d..ee5cce641c14 100644
--- a/Cargo.toml
+++ b/Cargo.toml
@@ -437,12 +437,25 @@ gc = ["wasmtime-cli-flags/gc"]
 
 # CLI subcommands for the `wasmtime` executable. See `wasmtime $cmd --help`
 # for more information on each subcommand.
-serve = ["wasi-http", "component-model", "dep:http-body-util", "dep:http"]
+serve = [
+  "wasi-http",
+  "component-model",
+  "dep:http-body-util",
+  "dep:http",
+  "wasmtime-cli-flags/async",
+]
 explore = ["dep:wasmtime-explorer", "dep:tempfile"]
 wast = ["dep:wasmtime-wast"]
 config = ["cache"]
 compile = ["cranelift"]
-run = ["dep:wasmtime-wasi", "wasmtime/runtime", "dep:listenfd", "dep:wasi-common", "dep:tokio"]
+run = [
+  "dep:wasmtime-wasi",
+  "wasmtime/runtime",
+  "dep:listenfd",
+  "dep:wasi-common",
+  "dep:tokio",
+  "wasmtime-cli-flags/async",
+]
 
 [[test]]
 name = "host_segfault"
diff --git a/crates/cli-flags/src/lib.rs b/crates/cli-flags/src/lib.rs
index ece1e20bcdf9..c8ff1e2c4290 100644
--- a/crates/cli-flags/src/lib.rs
+++ b/crates/cli-flags/src/lib.rs
@@ -202,6 +202,12 @@ wasmtime_option_group! {
         /// Maximum stack size, in bytes, that wasm is allowed to consume before a
         /// stack overflow is reported.
         pub max_wasm_stack: Option<usize>,
+        /// Stack size, in bytes, that will be allocated for async stacks.
+        ///
+        /// Note that this must be larger than `max-wasm-stack` and the
+        /// difference between the two is how much stack the host has to execute
+        /// on.
+        pub async_stack_size: Option<usize>,
         /// Allow unknown exports when running commands.
         pub unknown_exports_allow: Option<bool>,
         /// Allow the main module to import unknown functions, using an
@@ -658,8 +664,23 @@ impl CommonOptions {
             anyhow::bail!("memory protection keys require the pooling allocator");
         }
 
+        match_feature! {
+            ["async" : self.wasm.async_stack_size]
+            size => config.async_stack_size(size),
+            _ => err,
+        }
+
         if let Some(max) = self.wasm.max_wasm_stack {
             config.max_wasm_stack(max);
+
+            // If `-Wasync-stack-size` isn't passed then automatically adjust it
+            // to the wasm stack size provided here too. That prevents the need
+            // to pass both when one can generally be inferred from the other.
+            #[cfg(feature = "async")]
+            if self.wasm.async_stack_size.is_none() {
+                const DEFAULT_HOST_STACK: usize = 512 << 10;
+                config.async_stack_size(max + DEFAULT_HOST_STACK);
+            }
         }
 
         if let Some(enable) = self.wasm.relaxed_simd_deterministic {
diff --git a/tests/all/cli_tests.rs b/tests/all/cli_tests.rs
index a8743c910785..7f8b6b2f20fa 100644
--- a/tests/all/cli_tests.rs
+++ b/tests/all/cli_tests.rs
@@ -1098,6 +1098,21 @@ fn mpk_without_pooling() -> Result<()> {
     Ok(())
 }
 
+// Very basic use case: compile binary wasm file and run specific function with arguments.
+#[test]
+fn increase_stack_size() -> Result<()> {
+    run_wasmtime(&[
+        "run",
+        "--invoke",
+        "simple",
+        &format!("-Wmax-wasm-stack={}", 5 << 20),
+        "-Ccache=n",
+        "tests/all/cli_tests/simple.wat",
+        "4",
+    ])?;
+    Ok(())
+}
+
 mod test_programs {
     use super::{get_wasmtime_command, run_wasmtime};
     use anyhow::{bail, Context, Result};