diff --git a/crates/wasi/src/preview2/ctx.rs b/crates/wasi/src/preview2/ctx.rs
index d56f51a240dd..90ed5678aafd 100644
--- a/crates/wasi/src/preview2/ctx.rs
+++ b/crates/wasi/src/preview2/ctx.rs
@@ -1,10 +1,9 @@
 use super::clocks::host::{monotonic_clock, wall_clock};
 use crate::preview2::{
     bindings::cli::{terminal_input, terminal_output},
-    bindings::filesystem::types::Descriptor,
     bindings::io::streams,
     clocks::{self, HostMonotonicClock, HostWallClock},
-    filesystem::{Dir, TableFsExt},
+    filesystem::Dir,
     pipe, random, stdio,
     stdio::{HostTerminalInputState, HostTerminalOutputState},
     stream::{HostInputStream, HostOutputStream, TableStreamExt},
@@ -317,16 +316,6 @@ impl WasiCtxBuilder {
         let stdout = Some(table.push_output_stream(stdout.0).context("stdout")?);
         let stderr = Some(table.push_output_stream(stderr.0).context("stderr")?);
 
-        let preopens = preopens
-            .into_iter()
-            .map(|(dir, path)| {
-                let dirfd = table
-                    .push_dir(dir)
-                    .with_context(|| format!("preopen {path:?}"))?;
-                Ok((dirfd, path))
-            })
-            .collect::<anyhow::Result<Vec<_>>>()?;
-
         Ok(WasiCtx {
             stdin,
             stdin_terminal,
@@ -362,7 +351,7 @@ pub struct WasiCtx {
     pub(crate) monotonic_clock: Box<dyn HostMonotonicClock + Send + Sync>,
     pub(crate) env: Vec<(String, String)>,
     pub(crate) args: Vec<String>,
-    pub(crate) preopens: Vec<(Resource<Descriptor>, String)>,
+    pub(crate) preopens: Vec<(Dir, String)>,
     pub(crate) stdin: Option<Resource<streams::InputStream>>,
     pub(crate) stdout: Option<Resource<streams::OutputStream>>,
     pub(crate) stderr: Option<Resource<streams::OutputStream>>,
diff --git a/crates/wasi/src/preview2/filesystem.rs b/crates/wasi/src/preview2/filesystem.rs
index 27dd9d97303b..3f3cfb1b4329 100644
--- a/crates/wasi/src/preview2/filesystem.rs
+++ b/crates/wasi/src/preview2/filesystem.rs
@@ -93,6 +93,7 @@ bitflags::bitflags! {
     }
 }
 
+#[derive(Clone)]
 pub(crate) struct Dir {
     pub dir: Arc<cap_std::fs::Dir>,
     pub perms: DirPerms,
diff --git a/crates/wasi/src/preview2/host/filesystem.rs b/crates/wasi/src/preview2/host/filesystem.rs
index 36fc6c68e410..374d4a455fa5 100644
--- a/crates/wasi/src/preview2/host/filesystem.rs
+++ b/crates/wasi/src/preview2/host/filesystem.rs
@@ -6,6 +6,7 @@ use crate::preview2::bindings::filesystem::{preopens, types};
 use crate::preview2::bindings::io::streams;
 use crate::preview2::filesystem::{Dir, File, TableFsExt};
 use crate::preview2::{DirPerms, FilePerms, Table, TableError, WasiView};
+use anyhow::Context;
 use wasmtime::component::Resource;
 
 use types::ErrorCode;
@@ -22,12 +23,15 @@ impl<T: WasiView> preopens::Host for T {
     fn get_directories(
         &mut self,
     ) -> Result<Vec<(Resource<types::Descriptor>, String)>, anyhow::Error> {
-        Ok(self
-            .ctx_mut()
-            .preopens
-            .drain(..)
-            .map(|(fd, name)| (Resource::new_own(fd.rep()), name.clone()))
-            .collect())
+        let mut results = Vec::new();
+        for (dir, name) in self.ctx().preopens.clone() {
+            let fd = self
+                .table_mut()
+                .push_dir(dir)
+                .with_context(|| format!("failed to push preopen {name}"))?;
+            results.push((fd, name));
+        }
+        Ok(results)
     }
 }