diff --git a/internal/devbox/devbox.go b/internal/devbox/devbox.go
index 4c3f82421ce..e964ca7d67e 100644
--- a/internal/devbox/devbox.go
+++ b/internal/devbox/devbox.go
@@ -738,6 +738,15 @@ func (d *Devbox) computeEnv(
 		for k, v := range nixEnv {
 			env[k] = v
 		}
+
+		// The Nix dev-env sets the SSL certificate-bundle variables to a Nix
+		// store path whenever a package pulls in nss-cacert (e.g. httpie,
+		// python). That clobbers a value the user deliberately set in their own
+		// environment — most importantly a corporate MITM/proxy CA bundle —
+		// breaking outbound TLS for the rest of the project. Restore the user's
+		// own value so custom CA bundles keep working, mirroring how `nix shell`
+		// leaves these untouched. See jetify-com/devbox#2604.
+		preserveUserSSLCertFiles(env, originalEnv)
 	}
 	slog.Debug("nix environment PATH", "path", env["PATH"])
 
@@ -1100,6 +1109,27 @@ var ignoreDevEnvVar = map[string]bool{
 	"UID":                true,
 }
 
+// sslCertFileEnvVars are the certificate-bundle environment variables that
+// Nix's build environment sets (via packages such as nss-cacert, pulled in by
+// httpie, python, etc.). They point at a Nix store CA bundle, which is the right
+// default when the user hasn't set one themselves but is wrong when they have:
+// a user who exports one of these — typically to a corporate MITM/proxy CA
+// bundle — needs that value preserved for outbound TLS to keep working.
+var sslCertFileEnvVars = []string{"NIX_SSL_CERT_FILE", "SSL_CERT_FILE"}
+
+// preserveUserSSLCertFiles restores the user's own certificate-bundle variables
+// (taken from userEnv, the ambient environment captured before the Nix dev-env
+// is layered on) into env, so that a value the user explicitly set wins over the
+// Nix store path injected by the dev-env. Variables the user did not set are
+// left as-is, keeping the Nix default. See jetify-com/devbox#2604.
+func preserveUserSSLCertFiles(env, userEnv map[string]string) {
+	for _, key := range sslCertFileEnvVars {
+		if val, ok := userEnv[key]; ok && val != "" {
+			env[key] = val
+		}
+	}
+}
+
 func (d *Devbox) ProjectDirHash() string {
 	return cachehash.Bytes([]byte(d.projectDir))
 }
diff --git a/internal/devbox/devbox_test.go b/internal/devbox/devbox_test.go
index b0429dfd0d2..69e1e549a51 100644
--- a/internal/devbox/devbox_test.go
+++ b/internal/devbox/devbox_test.go
@@ -120,6 +120,68 @@ func TestComputeDevboxPathWhenRemoving(t *testing.T) {
 	assert.NotEqual(t, path, path2, "path should not be the same")
 }
 
+// testNixVars is a nix.Nixer mock whose PrintDevEnv returns a configurable set
+// of exported variables. Used to exercise how computeEnv layers the Nix
+// dev-env on top of the ambient environment.
+type testNixVars struct {
+	vars map[string]string
+}
+
+func (n *testNixVars) PrintDevEnv(ctx context.Context, args *nix.PrintDevEnvArgs) (*nix.PrintDevEnvOut, error) {
+	variables := map[string]nix.Variable{}
+	for k, v := range n.vars {
+		variables[k] = nix.Variable{Type: "exported", Value: v}
+	}
+	return &nix.PrintDevEnvOut{Variables: variables}, nil
+}
+
+func TestPreserveUserSSLCertFiles(t *testing.T) {
+	const userBundle = "/Library/Application Support/Netskope/STAgent/data/nscacert_combined.pem"
+	const nixBundle = "/nix/store/abc-nss-cacert-3.108/etc/ssl/certs/ca-bundle.crt"
+
+	t.Run("restores user value when set", func(t *testing.T) {
+		env := map[string]string{"NIX_SSL_CERT_FILE": nixBundle, "SSL_CERT_FILE": nixBundle}
+		userEnv := map[string]string{"NIX_SSL_CERT_FILE": userBundle, "SSL_CERT_FILE": userBundle}
+		preserveUserSSLCertFiles(env, userEnv)
+		assert.Equal(t, userBundle, env["NIX_SSL_CERT_FILE"])
+		assert.Equal(t, userBundle, env["SSL_CERT_FILE"])
+	})
+
+	t.Run("keeps nix value when user did not set one", func(t *testing.T) {
+		env := map[string]string{"NIX_SSL_CERT_FILE": nixBundle}
+		preserveUserSSLCertFiles(env, map[string]string{})
+		assert.Equal(t, nixBundle, env["NIX_SSL_CERT_FILE"])
+	})
+
+	t.Run("ignores empty user value", func(t *testing.T) {
+		env := map[string]string{"NIX_SSL_CERT_FILE": nixBundle}
+		preserveUserSSLCertFiles(env, map[string]string{"NIX_SSL_CERT_FILE": ""})
+		assert.Equal(t, nixBundle, env["NIX_SSL_CERT_FILE"])
+	})
+}
+
+// TestComputeEnvPreservesUserSSLCertFile is a regression test for
+// jetify-com/devbox#2604: adding a package that pulls in nss-cacert (e.g.
+// httpie) must not clobber a NIX_SSL_CERT_FILE the user set in their own
+// environment (e.g. a corporate MITM CA bundle).
+func TestComputeEnvPreservesUserSSLCertFile(t *testing.T) {
+	const userBundle = "/Library/Application Support/Netskope/STAgent/data/nscacert_combined.pem"
+	const nixBundle = "/nix/store/abc-nss-cacert-3.108/etc/ssl/certs/ca-bundle.crt"
+
+	d := devboxForTesting(t)
+	d.nix = &testNixVars{vars: map[string]string{
+		"PATH":              "/tmp/my/path",
+		"NIX_SSL_CERT_FILE": nixBundle,
+	}}
+
+	t.Setenv("NIX_SSL_CERT_FILE", userBundle)
+
+	env, err := d.computeEnv(t.Context(), false /*use cache*/, devopt.EnvOptions{})
+	require.NoError(t, err, "computeEnv should not fail")
+	assert.Equal(t, userBundle, env["NIX_SSL_CERT_FILE"],
+		"the user's NIX_SSL_CERT_FILE should win over the nix dev-env value")
+}
+
 func devboxForTesting(t *testing.T) *Devbox {
 	path := t.TempDir()
 	_, err := devconfig.Init(path)